Publications

Journal names have been intentionally excluded. Lab member names are in bold. Links are provided to the published article and when possible an open-access version (pre- or post-print) of the paper. Click on a triangle for the article abstract.

Preprints

The utility of environmental data from traditional varieties for climate-adaptive maize breeding [preprint]
Li F, Gates DJ, Buckler ES, …[8 authors]… Hearne S, Ross-Ibarra J, Runcie DE

Maintaining crop yields in the face of climate change is a major challenge facing plant breeding today. Considerable genetic variation exists in ex-situ collections of traditional crop varieties, but identifying adaptive loci and testing their agronomic performance in large populations in field trials is costly. Here, we study the utility of climate and genomic data for identifying promising traditional varieties to incorporate into maize breeding programs. To do so, we use phenotypic data from more than 4,000 traditional maize varieties grown in 13 trial environments. First, we used genotype data to predict environmental characteristics of germplasm collections to identify varieties that may be locally adapted to target environments. Second, we used environmental GWAS (envGWAS) to identify genetic loci associated with historical divergence along climatic gradients, such as the putative heat shock protein Hsftf9 and the large-scale adaptive inversion Inv4m. Finally, we compared the value of environmental data and envGWAS-prioritized loci to genomic data for prioritizing traditional varieties. We find that maize yield traits are best predicted by genomic data, and that envGWAS-identified variants provide little direct predictive information over patterns of population structure. We also find that adding environment-of-origin variables does not improve yield component prediction over kinship or population structure alone, but could be a useful selection proxy in the absence of sequencing data. While our results suggest little utility of environmental data for selecting traditional varieties to incorporate in breeding programs, environmental GWAS is nonetheless a potentially powerful approach to identify individual novel loci for maize improvement, especially when coupled with high density genotyping.

A unified VCF data set from nearly 1,500 diverse maize accessions and resources to explore the genomic landscape of maize [preprint]
Andorf CM, Ross-Ibarra J, Seetharam AS, Hufford MB, Woodhouse MR

Efforts to capture and analyze maize nucleotide diversity have ranged widely in scope, but differences in reference genome version and software algorithms used in these efforts inhibit comparison. To address these continuity issues, The Maize Genetics and Genomics Database has collaborated with researchers in the maize community to offer variant data from a diverse set of 1,498 inbred lines, traditional varieties, and teosintes through a standardized variant-calling pipeline against version 5 of the B73 reference genome. The output was filtered for mapping quality, coverage, and linkage disequilibrium, and annotated based on variant effects relative to the B73 RefGen_v5 gene annotations. MaizeGDB has also updated a web tool to filter, visualize, and download genotype sets based on genomic locations and accessions of interest. MaizeGDB plans to host regular updates of these resources as additional resequencing data become available, with plans to expand to all publicly available sequence data.

Phenotypic variation in maize can be largely explained by genetic variation at transcription factor binding sites [preprint]
Engelhorn J, Snodgrass SJ, Kok A, Seetharam AS, …[15 authors]… Frommer WB, Ross-Ibarra J, Hartwig T

Comprehensive maps of functional variation at transcription factor (TF) binding sites (cis-elements) are crucial for elucidating how genotype shapes phenotype. Here we report the construction of a pan-cistrome of the maize leaf under well-watered and drought conditions. We quantified haplotype-specific TF footprints across a pan-genome of 25 maize hybrids and mapped nearly two-hundred thousand genetic variants (termed binding-QTLs) linked to cis-element occupancy. The functional significance of binding-QTLs is supported by three lines of evidence: i) they coincide with known causative loci that regulate traits, including novel alleles of Upright Plant Architecture2, Trehalase1, and the MITE transposon site of ZmNAC111 under drought; ii) their allelic bias is mirrored between inbred parents and by ChIP-seq; iii) partitioning genetic variation across genomic regions demonstrates that binding-QTLs capture the majority of heritable trait variation across ~70% of 143 phenotypes. Our study provides a promising approach to make previously hidden cis-variation more accessible for genetic studies and multi-target engineering of complex traits.

2024

Teosinte populations exhibit weak local adaptation to their rhizosphere biota despite strong effects of biota source on teosinte fitness and traits [preprint]
O’Brien AM, Sawers RJH, Gasca-Pineda J, Baxter, I, Eguiarte LE, Ross-Ibarra J, Strauss SY

While biotic interactions often impose selection, species and populations vary in whether they are locally adapted to biotic interactions. Evolutionary theory predicts that environmental conditions drive this variable local adaptation by altering the fitness impacts of species interactions. To investigate the influence of an environmental gradient on adaptation between a plant and its associated rhizosphere biota, we cross-combined teosinte Zea mays ssp. mexicana) and rhizosphere biota collected across a gradient of decreasing temperature, precipitation, and nutrients in a greenhouse common garden experiment. We measured both fitness and phenotypes expected to be influenced by biota, including concentrations of nutrients in leaves. Independent, main effects of teosinte and biota source explained most variation in teosinte fitness and traits. For example, biota from warmer sites provided population-independent fitness benefits across teosinte hosts. Effects of biota that depended on teosinte genotype were often not specific to their local hosts, and most traits had similar relationships to fitness across biota treatments. However, we found weak patterns of local adaptation between teosinte and biota from colder sites, suggesting environmental gradients may alter the importance of local adaptation in teosinte-biota interactions, as evolutionary theory predicts.

Teosinte Pollen Drive guides maize domestication and evolution by RNAi [preprint]
Berube B, Ernst E, Cahn J, …[3 authors]… Scheben A, Siepel A, Ross-Ibarra J, Kermicle J, Martienssen RA.

Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Using single molecule and single-pollen genome sequencing, we describe Teosinte Pollen Drive, an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi). 22nt small RNAs from a non-coding RNA hairpin in mexicana depend on Dicer-Like 2 (Dcl2) and target Teosinte Drive Responder 1 (Tdr1), which encodes a lipase required for pollen viability. Dcl2, Tdr1, and the hairpin are in tight pseudolinkage on chromosome 5, but only when transmitted through the male. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas, and a tightly linked inversion in mexicana spans a major domestication sweep in modern maize. A survey of maize landraces and sympatric populations of teosinte mexicana reveals correlated patterns of admixture among unlinked genes required for RNAi on at least 3 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication and evolution, and offers an explanation for the widespread abundance of “self” small RNAs in the germlines of plants and animals.

Other papers by lab members

Alyssa Phillips

 Current genomic deep learning architectures generalize across grass species but not alleles. Travis Wrightsman, Taylor H. Ferebee, M. Cinta Romay, Taylor AuBuchon-Elder, Alyssa R. Phillips, Michael Syring, Elizabeth A. Kellogg, Edward S. Buckler. bioRxiv 2024.04.11.589024; doi: https://doi.org/10.1101/2024.04.11.589024   
  
  Phillips, A. R. 2024. Variant calling in polyploids for population and quantitative genetics. Applications in Plant Sciences 12(4): e11607. https://doi.org/10.1002/aps3.11607

2023

Two teosintes made modern maize. [preprint]
Yang N*, Wang Y*, Liu X* …[20 authors including Mambakkam M and Menon M]… Stitzer MC, Runcie DE, Yan J, Ross- Ibarra J

Despite its global importance as a crop with broad economic, dietary, and cultural importance, the origins of maize and its closest wild relatives remained the topic of vigorous debate for nearly a century. Molecular analyses ultimately concluded that maize was domesticated once from a common ancestor with its closest extant relative, the lowland wild grass Zea mays ssp. parviglumis. But neither the current genetic model nor earlier models based on archaeological data account for the totality of available data, and recent work has highlighted the potential contribution of a second wild relative, the highland Zea mays ssp. mexicana. Here we present a detailed population genetic analysis of the contributions of both wild taxa to modern maize diversity using the largest sample of traditional maize varieties sequenced to date. We show that all modern maize can trace its origin to an ancient admixture event between domesticated ancient maize and Zea mays ssp. mexicana in the highlands of Mexico ca 5300 cal BP, some 4,000 years after domestication began. We show that variation in admixture is a key component of modern maize genetic and phenotypic diversity, both at the level of individual loci and as a factor driving a substantial component of additive genetic variation across a number of agronomic traits. Our results clarify the long-debated origin of modern maize, highlight the potential contributions of crop wild relatives to agronomic improvement, and raise new questions about the anthropogenic mechanisms underlying multiple waves of dispersal throughout the Americas.

Not so local: the population genetics of convergent adaptation in maize and teosinte. [preprint]
Tittes S, Lorant A, McGinty S, …[4 authors]… Tenaillon MI, Ross-Ibarra J

What is the genetic architecture of local adaptation and what is the geographic scale that it operates over? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are frequently shared by several populations, and often between the subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, post domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, out results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations, but smaller than the species range.

Genetic modification can improve crop yields — but stop overselling it
Khaipho-Burch M, Cooper M, Crossa J, de Leon N …[5 authors]… Ronald P, Ross-Ibarra J, Weigel D, Buckler ES

With a changing climate and a growing population, the world increasingly needs more-productive and resilient crops. But improving them requires a knowledge of what actually works in the field.

Unraveling prevalence and effects of deleterious mutations in maize elite lines across decades of modern breeding
Sun S, Wang B, Li C, Xu G, Yang J, Hufford MBH, Ross-Ibarra J, Wang H, Wang L

Future breeding is likely to involve the detection and removal of deleterious alleles, which are mutations that negatively affect crop fitness. However, little is known about the prevalence of such mutations and their effects on phenotypic traits in the context of modern crop breeding. To address this, we examined the number and frequency of deleterious mutations in 350 elite maize inbred lines developed over the past few decades in China and the United States. Our findings reveal an accumulation of weakly deleterious mutations and a decrease in strongly deleterious mutations, indicating the dominant effects of genetic drift and purifying selection for the two types of mutations, respectively. We also discovered that slightly deleterious mutations, when at lower frequencies, were more likely to be heterozygous in the developed hybrids. This is consistent with complementation as a potential explanation for heterosis. Subsequently, we found that deleterious mutations accounted for more of the variation in phenotypic traits than non-deleterious mutations with matched minor allele frequencies, especially for traits related to leaf angle and flowering time. Moreover, we detected fewer deleterious mutations in the promoter and gene body regions of differentially expressed genes across breeding eras than in non-differentially expressed genes. Overall, our results provide a comprehensive assessment of the prevalence and impact of deleterious mutations in modern maize breeding and establish a useful baseline for future maize improvement efforts.

Diamonds in the Not-So-Rough: Wild Relative Diversity Hidden in Crop Genomes [preprint]
Flint-Garcia S, Hannes Dempewolf H, Feldmann MJ, Morrell PL, Ross-Ibarra J

Cultivated species have reduced genetic diversity relative to their closest wild relatives. Domestication also changes the type and effect of polymorphic variants in domesticates. Cultivated species selected for productivity under optimal growth environments have often lost genetic variants that contributed to adaptation to diverse and now rapidly changing environments. Selection for yield can also cause harmful variants segregating in wild relative populations to either be lost to purifying selection or fixed in domesticates. Preservation and effective utilization of the rich genetic resources that crop wild relatives offer while avoiding detrimental variants and maladaptive genetic contributions is a central challenge for ongoing crop improvement. Most crops show evidence of admixture and gene flow with their wild relatives during the course of evolution. We argue that allelic diversity from crop wild relatives likely already exists in cultivated populations conserved in germplasm repositories. These alleles have been tested by evolution in an agronomic background. Many are of sufficient age that the twofold sieve of recombination and selection have separated them from linked deleterious variants. Surveying domesticated traditional varieties for functionally relevant variation from wild relatives may thus greatly facilitate the identification and incorporation of useful wild diversity into modern breeding programs.

A happy accident: a novel turfgrass reference genome [preprint]
Phillips AR*, Seetharam AR*, AuBuchon-Elder T …[6 authors]… Kellogg E, Ross-Ibarra J

Poa pratensis, commonly known as Kentucky bluegrass, is a popular cool-season grass species used as turf in lawns and recreation areas globally. Despite its substantial economic value, a reference genome had not previously been assembled due to the genome’s relatively large size and biological complexity that includes apomixis, polyploidy, and interspecific hybridization. We report here a fortuitous de novo assembly and annotation of a P. pratensis genome. The draft assembly consists of 6.09 Gbp with an N50 scaffold length of 65.1 Mbp, and a total of 118 scaffolds, generated using PacBio long reads and Bionano optical map technology. We annotated 256K gene models and found 58% of the genome to be composed of transposable elements. To demonstrate the applicability of the reference genome, we evaluated population structure and estimated genetic diversity in three North American wild P. pratensis populations. Our results support previous studies that found high genetic diversity and population structure within the species. The reference genome and annotation will be an important resource for turfgrass breeding and biologists interested in this complex species.

Other papers by lab members

Regina Fairbanks

DiVito Evans, A., Fairbanks, R. A., Schmidt, P., & Levine, M. T. (2023). Histone methylation regulates reproductive diapause in Drosophila melanogaster. PLoS genetics, 19(9), e1010906. 

Mitra Menon

Sun, X., Xiang, Y., Dou, N. et al. The role of transposon inverted repeats in balancing drought tolerance and yield-related traits in maize. Nat Biotechnol 41, 120–127 (2023). 

2022

Allele-specific expression reveals multiple paths to highland adaptation in maize [preprint]
Hu H, Crow T, Nojoomi S, …[5 authors]… Estévez-Palmas JM, Ross-Ibarra J, Runcie DE.

Maize is a staple food of smallholder farmers living in highland regions up to 4,000 meters above sea level worldwide, and Mexican and South American highlands are two major highland maize growing regions. Maize landraces show numerous adaptations to highland environments, and population genetic data suggests the highland populations largely independently from local lowland populations on each continent. To better understand the mechanistic basis of highland adaptation, we crossed maize landraces from 108 highland and lowland sites of Mexico and South America (MSA) with the inbred line B73 to produce F1 hybrids and grew them in both highland and lowland sites in Mexico. We identified thousand of genes with divergent expression between highland and lowland populations. Hundreds of these genes show patterns of convergent evolution etween Mexico and South America, including 17 flowering-related genes. To dissect the genetic architecture of the divergent gene expression, we developed a novel allele-specific expression analysis pipeline to detect genes with divergent functional cis-regulatory variation between highland and lowland populations. We identified hudnreds of genes with divergent cis-regulation between highland and lowland landrace alleles, with 20 in common between regions, further suggesting convergence in the genes underlying adaptation. Principal component analyses of these 20 loci provided evidence of multiple mechanisms underlying this convergent adaptation: the spread of adaptive allele through migration and the recruitment of different, but functionally similar, alleles in different populations. Our findings reveal a complex genetic architecture of cis-regulatory alleles underlying adaptation to highlands in maize. Although the vast majority of evolutionary changes associated with highland adaptation were region-specific, our findings highlight an important role for convergence at the gene expression and gene regulation levels as well.

Conflict over fertilization underlies the transient evolution of reinforcement. [preprint]
Rushworth C, Wardlaw AW, Ross-Ibarra J, Brandvain YB.

When two populations or species hybridize, their offspring often experience reductions in fitness relative to either parental population. The production of low fitness hybrids may be prevented by the evolution of increased prezygotic isolation; a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem — e.g., linkage disequilibrium between trait and preference loci is difficult to maintain in the face of recombination. However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for postmating prezygotic isolation, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. Motivated by this problem, we develop a population genetic model of interspecific conflict over reinforcement, inspired by `gametophytic factors’, which act as postmating prezygotic barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement –– after female preference for a conspecific gamete trait rises to high frequency, male traits adaptively introgress into the other population. Ultimately the male gamete trait fixes in both species, and prezygotic isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z. mays subspecies in light of these findings, and suggest when and how this conflict can be mediated. Our results suggest that sexual conflict may pose an understudied obstacle to the evolution of reinforcement via postmating prezygotic isolation.

Genome sequencing reveals evidence of adaptive variation in the genus Zea [preprint]
Chen L, Luo J, Minliang Jin, Yang N …[27 authors including Phillips AR and Cameron B]… Ross-Ibarra J, Yan J.

Maize is a globally valuable commodity and one of the most extensively studied genetic model organisms. However, we know surprisingly little about the extent and potential utility of the genetic variation found in the wild relatives of maize. Here, we characterize a high-density genomic variation map from 744 genomes encompassing maize and all wild taxa of the genus Zea, identifying over 70 million single nucleotide polymorphisms (SNPs) and nearly 9 million Insertion/Deletion (InDel) polymorphisms. The variation map reveals evidence of selection within taxa displaying novel adaptations to traits such as waterlogging, perenniality and regrowth. We focus in detail on adaptive alleles in highland teosinte and temperate maize and highlight the key role of flowering time related pathways in highland and high latitude adaptation. To show how this data can identify useful genetic variants, we generated and characterized novel mutant alleles for two flowering time candidate genes. This work provides the most extensive sampling to date of the genetic diversity of the genus Zea, resolving questions on evolution and identifying adaptive variants for direct use in modern breeding.

Genomic Insights into Historical Improvement of Heterotic Groups during Modern Hybrid Maize Breeding
Li C, Guan H, Jing X, Li Y …[18 authors]… Ross-Ibarra J, Li Y, Wang T, Wang H

Single-cross maize hybrids display superior heterosis and are produced from crossing two parental inbred lines belonging to genetically different heterotic groups. To dissect the genomic basis underlying breeding improvement of heterotic groups, we assembled 1,604 historically utilized maize inbred lines belonging to various female and male heterotic groups, and conducted phenotyping and genomic sequencing analyses. We find that the female heterotic groups (FHGs) and male heterotic groups (MHGs) have undergone convergent changes in a common set of plant architecture- and yield-related traits across the breeding eras for increased tolerance to higher planting density and increased yield. In addition, we find that the FHGs and MHGs have experienced divergent changes for three ear-related traits associated with kernel dehydration rate and mechanical harvesting. Using genome-wide selection scans and association analyses, we identify a large number of candidate genes that contributed to the improvement of agronomic traits of the female and male parental lines. Moreover, we observe increased genetic differentiation between the FHGs and MHGs across the breeding eras, and find positive correlation between increase of heterozygosity levels in the differentiated genes with heterosis in hybrids. Further, we validate the function of two selected genes affecting flowering time/ear height and kernel length/kernel weight in inbred lines, and a differentiated gene promoting ear length/ear weight in hybrids. This study provides insights into the genomic basis of hybrid maize breeding, and should enable future genomics-informed maize breeding.

The genomic signature of wild-to-crop introgression during the domestiation of scarlet runner bean (Phaseolus coccineus L.) [preprint]
Guerra-Garcia A, Rojas-Barrera IC, Ross-Ibarra J, Papa R, Piñero D.

The scarlet runner bean is an open-pollinated legume from the highlands of Mesoamerica that is cultivated in small-scale agriculture for its dry seeds and immature pods. Demographic bottlenecks associated with domestication might reduce genetic diversity and facilitate the accumulation of deleterious mutations. Conversely, introgression from wild relatives could be a source of variation. Using Genotyping by Sequencing data (79,286 SNVs) from 237 cultivated and wild samples, we evaluated the demographic history of traditional varieties from different regions of Mexico and looked for evidence of introgression between sympatric wild and cultivated populations. Traditional varieties have high levels of diversity, even though there is evidence of a severe initial genetic bottleneck, followed by a population expansion. Introgression from wild to domesticated populations was detected, but not in the opposite direction. This asymmetric introgression might contribute to the recovery of genetic variation and it has occurred at different times: constantly in the center of Mexico; recently in the North West; and anciently in the South. Several factors are acting together to increase and maintain genetic diversity in P. coccineus cultivars, such as demographic expansion and introgression. Wild relatives represent a valuable genetic resource and have played a key role in scarlet runner bean evolution via introgression into traditional varieties.

An adaptive teosinte mexicana introgression modulates phosphatidylcholine levels and is associated with maize flowering time [preprint]
Barnes AC*, Rodríguez-Zapata F*, Blöcher-Juárez KA*, Gates DJ …[22 authors]… Ross-Ibarra J, Hufford M, Sawers RJH, Rellán-Álvarez R.

Native Americans domesticated maize (Zea mays ssp. mays) from lowland teosinte parviglumis (Zea mays ssp.parviglumis) in the warm Mexican southwest and brought it to the highlands of México and South America where it was exposed to lower temperatures that imposed strong selection on flowering time. Phospholipids are important metabolites in plant responses to low-temperature and phosphorus availability, and have been suggested to influence flowering time. Here, we combined linkage mapping with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene that encodes a phospholipase A1 enzyme, as a major driver of phospholipid variation in highland maize. Common garden experiments demonstrated strong genotype-by-environment interactions associated with variation at HPC1, with the highland HPC1 allele leading to higher fitness in highlands, possibly by hastening flowering. The highland maize HPC1 variant resulted in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis across HPC1 orthologs indicated a strong association between the identity of the amino acid at this position and optimal growth in prokaryotes. Mutagenesis of HPC1 via genome editing validated its role in regulating phospholipid metabolism. Finally, we showed that the highland HPC1 allele entered cultivated maize by introgression from the wild highland teosinte Zea mays ssp. mexicana and has been maintained in maize breeding lines from the Northern US, Canada and Europe. Thus, HPC1 introgressed from teosinte mexicana underlies a large metabolic QTL that modulates phosphatidylcholine levels and has an adaptive effect at least in part via induction of early flowering time.

Controlling for variable transposition rate with an age-adjusted site frequency spectrum [preprint]
Horvath R, Menon M, Stitzer MC, Ross-Ibarra J

Recognition of the important role of transposable elements (TEs) in eukaryotic genomes quickly led to a burgeoning literature modeling and estimating the effects of selection on TEs. Much of the empirical work on selection has focused on analyzing the site frequency spectrum (SFS) of TEs. But TEs differ from standard evolutionary models in a number of ways that can impact the power and interpretation of the SFS. For example, rather than mutating under a clock-like model, transposition often occurs in bursts which can inflate particular frequency categories compared to expectations under a standard neutral model. If a TE burst has been recent, the excess of low frequency polymorphisms can mimic the effect of purifying selection. Here, we investigate how transposition bursts affect the frequency distribution of TEs and the correlation between age and allele frequency. Using information on the TE age distribution, we propose an age-adjusted site frequency spectrum to compare TEs and neutral polymorphisms to more effectively evaluate whether TEs are under selective constraints. We show that our approach can minimize instances of false inference of selective constraint, but also allows for a correct identification of even weak selection affecting TEs which experienced a transposition burst and is robust to at least simple demographic changes. The results presented here will help researchers working on TEs to more reliably identify the effects of selection on TEs without having to rely on the assumption of a constant transposition rate.

Analysis of genotype by environment interactions in a maize mapping population [preprint]
Hudson AI, Odell SG, Dubreuil P, Tixier M-H, Praud S, Runcie DE, Ross-Ibarra J

Genotype by environment interactions are a significant challenge for crop breeding as well as being important for understanding the genetic basis of environmental adaptation. In this study, we analyzed genotype by environment interaction in a maize multi-parent advanced generation intercross population grown across five environments. We found that genotype by environment interactions contributed as much as genotypic effects to the variation in some agronomically important traits. In order to understand how genetic correlations between traits change across environments, we estimated the genetic variance-covariance matrix in each environment. Changes in genetic covariances between traits across environments were common, even among traits that show low genotype by environment variance. We also performed a genome-wide association study to identify markers associated with genotype by environment interactions but found only a small number of significantly associated markers, possibly due to the highly polygenic nature of genotype by environment interactions in this population.

Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte [preprint]
Holland JB, Samayoa LF, Olukolu BA, Yang CJ, …[7 authors]… Yang J, Ross-Ibarra J, Buckler ES, Doebley JF.

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to rare large-effect variation versus potentially more common variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load predicted from sequence data in the maize population. For many traits - and more commonly in maize - genetic variation among self-fertilized families was less than expected based on additive and dominance variance estimated in outcrossed families, suggesting that a negative covariance between additive and homozygous dominance effects limits the variation available to selection under partial inbreeding. We identified quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, small-effect recessive variation underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following to the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against large effect variants, but polygenic load is harder to purge and segregating mutational burden increased in maize compared to teosinte.

A B73 x Palomero Toluqueo mapping population reveals local adaptation in Mexican highland maize [preprint]
Perez-Limon S, Li M, …[13 authors]… Ross-Ibarra J, Flint-Garcia S, Diaz-Garcia L, Rellán-Álvarez R, Sawers RJH

Generations of farmer selection have produced a unique collection of traditional maize varieties adapted to the environmental challenges of the central Mexican highlands. In addition to agronomic and cultural value, Mexican highland maize represents a good system for the study of local adaptation and acquisition of adaptive phenotypes under cultivation. In this study, we characterized a recombinant inbred line population derived from the cross of the B73 reference line and the Mexican highland maize variety Palomero Toluqueo. Evaluation over multiple years in lowland and highland field sites in Mexico identified genomic regions linked to yield components and putatively adaptive morphological traits. A region on chromosome 7 associated with ear weight showed antagonistic allelic effects in lowland and highland fields, suggesting a trade-off consistent with local adaptation. We identified several alleles of highland origin associated with characteristic highland traits, including reduced tassel branching, increased stem pigmentation and the presence of stem macrohairs. The oligogenic architecture of characteristic morphological traits supports their role in adaptation, suggesting they have arisen from consistent directional selection acting at distinct points across the genome. We discuss these results in the context of the origin of phenotypic novelty during selection, commenting on the role of de novo mutation and the acquisition of adaptive variation by gene flow from endemic wild relatives.

Other papers by lab members

2021

Modeling Allelic Diversity of Multi-parent Mapping Populations Affects Detection of Quantitative Trait Loci [preprint]
Odell SG, Hudson AI, Praud S, Dubreuil P, Tixier M-H, Ross-Ibarra J, Runcie DE

The search for quantitative trait loci (QTL) that explain complex traits such as yield and flowering time has been ongoing in all crops. Methods such as bi-parental QTL mapping and genome-wide association studies (GWAS) each have their own advantages and limitations. Multi-parent advanced generation intercross (MAGIC) populations contain more recombination events and genetic diversity than bi-parental mapping populations and reduce the confounding effect of population structure that is an issue in association mapping populations. Here we discuss the results of using a MAGIC population of doubled haploid (DH) maize lines created from 16 diverse founders to perform QTL mapping. We compare three models that assume bi-allelic, founder, and ancestral haplotype allelic states for QTL. The three methods have different power to detect QTL for a variety of agronomic traits. Although the founder approach finds the most QTL, there are also QTL unique to each method, suggesting that each model has advantages for traits with different genetic architectures. A closer look at a well-characterized flowering time QTL, qDTA8, which contains vgt1, suggests a potential epistatic interaction and highlights the strengths and weaknesses of each method. Overall, our results reinforce the importance of considering different approaches to analyzing genotypic datasets, and show the limitations of binary SNP data for identifying multi-allelic QTL.

Selective sorting of ancestral introgression in maize and teosinte along an elevational cline [preprint]
Calfee E, Gates DJ, Lorant A, Perkins MT, Coop G, Ross-Ibarra J.

While often deleterious, hybridization can also be a key source of genetic variation and pre-adapted haplotypes, enabling rapid evolution and niche expansion. Here we evaluate these opposing selection forces on introgressed ancestry between maize (Zea mays ssp. mays), and its wild teosinte relative. Introgression from ecologically diverse teosinte may have facilitated maize’s global range expansion, in particular to challenging high elevation regions (> 1500 m). We generated low-coverage genome sequencing data for 348 maize and mexicana individuals to evaluate patterns of introgression in 14 sympatric population pairs, spanning the elevational range of Zea mays ssp. mexicana, a teosinte endemic to the mountains of Mexico. While recent hybrids are commonly observed in sympatric populations and mexicana demonstrates fine-scale local adaptation, we find that the majority of mexicana ancestry tracts introgressed >1000 generations ago. This mexicana ancestry seems to have maintained much of its diversity and likely came from a common ancestral source, rather than contemporary sympatric populations, resulting in relatively low Fst between mexicana ancestry tracts sampled from geographically distant maize populations. Introgressed mexicana ancestry is reduced in lower-recombination rate quintiles of the genome and around domestication genes, consistent with pervasive selection against introgression. However, we also find mexicana ancestry increases across the sampled elevational gradient and that high introgression peaks are most commonly shared among high-elevation maize populations, consistent with introgression from mexicana facilitating adaptation to the highland environment. In the other direction, we find patterns consistent with adaptive and clinal introgression of maize ancestry into sympatric mexicana at many loci across the genome, suggesting that maize also contributes to adaptation in mexicana, especially at the lower end of its elevational range. In sympatric maize, in addition to high introgression regions we find many genomic regions where selection for local adaptation maintains steep gradients in introgressed mexicana ancestry across elevation, including at least two inversions: the well-characterized Inv4m and a new 3 Mb inversion Inv9f surrounding the macrohairless1 locus on chromosome 9. The bulk of our ancestry selection outliers show no signals of sweeps or local sourcing from sympatric populations and so likely represent ancestral introgression sorted by selection, resulting in correlated but distinct outcomes of introgression in different contemporary maize landrace populations.

The Genomic Ecosystem of Transposable Elements in Maize [preprint][github][interactive]
Stitzer MC, Anderson SN, Springer NM, Ross-Ibarra J

Transposable elements (TEs) constitute the majority of flowering plant DNA, reflecting their tremendous success in subverting, avoiding, and surviving the defenses of their host genomes to ensure their selfish replication. More than 85% of the sequence of the maize genome can be ascribed to past transposition, providing a major contribution to the structure of the genome. Evidence from individual loci has informed our understanding of how transposition has shaped the genome, and a number of individual TE insertions have been causally linked to dramatic phenotypic changes. But genome-wide analyses in maize and other taxa have frequently represented TEs as a relatively homogeneous class of fragmentary relics of past transposition, obscuring their evolutionary history and interaction with their host genome. Using an updated annotation of structurally intact TEs in the maize reference genome, we investigate the family-level ecological and evolutionary dynamics of TEs in maize. Integrating a variety of data, from descriptors of individual TEs like coding capacity, expression, and methylation, as well as similar features of the sequence they inserted into, we model the relationship between these attributes of the genomic environment and the survival of TE copies and families. Our analyses reveal a diversity of ecological strategies of TE families, each representing the evolution of a distinct ecological niche allowing survival of the TE family. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences generate a rich ecology of the genome, suggesting families of TEs that coexist in time and space compete and cooperate with each other. We conclude that while the impact of transposition is highly family- and context-dependent, a family-level understanding of the ecology of TEs in the genome can refine our ability to predict the role of TEs in generating genetic and phenotypic diversity.

De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. [preprint]
Hufford MB, Seetharam AS, …[40 authors including Hudson AI and Tittes S]… Ross-Ibarra J, Yu J, Gent JI, Hirsch CN, Ware D, Dawe RK.

We report de novo genome assemblies, transcriptomes, annotations, and methylomes for the 26 inbreds that serve as the founders for the maize nested association mapping population. The data indicate that the number of pan-genes exceeds 103,000 and that the ancient tetraploid character of maize continues to degrade by fractionation to the present day. Excellent contiguity over repeat arrays and complete annotation of centromeres further reveal the locations and internal structures of major cytological landmarks. We show that combining structural variation with SNPs can improve the power of quantitative mapping studies. Finally, we document variation at the level of DNA methylation, and demonstrate that unmethylated regions are enriched for cis-regulatory elements that overlap QTL and contribute to changes in gene expression.

Conserved noncoding sequences provide insights into regulatory sequence and loss of gene expression in maize. [preprint]
Song B, Buckler ES, Wang H, Wu Y, …[4 authors including D Gates]… Bradbury PJ, Ross-Ibarra J, Hufford MB, Romay MC.

DNA sequencing technology has advanced so quickly, identifying key functional regions using evolutionary approaches is required to understand how those genomes work. This research develops a sensitive sequence alignment approach to identify functional constrained non-coding sequences in the Andropogoneae tribe. The grass tribe Andropogoneae contains several crop species descended from a common ancestor ~18 million years ago. Despite broadly similar phenotypes, they have tremendous genomic diversity with a broad range of ploidy levels and transposons. These features make Andropogoneae a powerful system for studying conserved non-coding sequence (CNS), here we used it to understand the function of CNS in maize. We find that 86% of CNS comprise known genomic elements e.g., cis-regulatory elements, chromosome interactions, introns, several transposable element superfamilies, and are linked to genomic regions related to DNA replication initiation, DNA methylation and histone modification. In maize, we show that CNSs regulate gene expression and variants in CNS are associated with phenotypic variance, and rare CNS absence contributes to loss of gene expression. Furthermore, we find the evolution of CNS is associated with the functional diversification of duplicated genes in the context of the maize subgenomes. Our results provide a quantitative understanding of constrained non-coding elements and identify functional non-coding variation in maize.

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces [preprint]
Wang L, Josephs EB, Lee KM, Roverts LM, Rellán-Álvarez R, Ross-Ibarra J, Hufford MB.

Convergent phenotypic evolution provides some of the strongest evidence for adaptation. However, the extent to which recurrent phenotypic adaptation has arisen via parallelism at the molecular level remains unresolved, as does the evolutionary origin of alleles underlying such adaptation. Here, we investigate genetic mechanisms of convergent highland adaptation in maize landrace populations and evaluate the genetic sources of recurrently selected alleles. Population branch excess statistics reveal strong evidence of parallel adaptation at the level of individual SNPs, genes and pathways in four independent highland maize populations, even though most SNPs show unique patterns of local adaptation. The majority of selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands. Polygenic adaptation analyses of quantitative traits reveal that alleles affecting flowering time are significantly associated with elevation, indicating the flowering time pathway was targeted by highland adaptation. In addition, repeatedly selected genes were significantly enriched in the flowering time pathway, indicating their significance in adapting to highland conditions. Overall, our study system represents a promising model to study convergent evolution in plants with potential applications to crop adaptation across environmental gradients.

Gene body methylation is under selection in Arabidopsis thaliana. [preprint]
Muyle A, Ross-Ibarra J, Seymour DK, Gaut BS.

In plants, mammals and insects, some genes are DNA methylated in the CG dinucleotide context, a phenomenon called gene body methylation. It has long been controversial whether this phenomenon has any functional role. Here, we took advantage of the availability of 868 leaf methylomes in Arabidopsis thaliana to characterize the population frequency of gene body methylation at the gene level. We used two outgroups to infer the ancestral methylation state of orthologs. Using the A. thaliana gene body methylation site frequency spectrum and a population genetics model specifically designed for epigenetic data, we find that genes with ancestral gene body methylation are under significant selection to remain methylated. Conversely, ancestrally unmethylated genes are under selection to remain unmethylated. The estimated selection coefficients are small, on the order of magnitude of selection acting on codon usage. We also find that A. thaliana is losing gene body methylation more often than gaining it, which could be due to a recent reduction in the efficacy of selection after a switch to selfing. We investigated the potential function of gene body methylation through its link with gene expression level. We show that, within genes with polymorphic methylation states in A. thaliana wild populations, the gene body methylated state is consistently associated with the highest gene expression level. Our work suggests that gene body methylation has a small effect on fitness, but substantial enough for natural selection to act on it.

Comparative evolutionary analysis and prediction of deleterious mutation patterns between sorghum and maize [preprint][github]
Lozano R, Gazave E, dos Santos JPR, Stetter MG …[4 authors]… Mockler T, Buckler ES, Ross-Ibarra J, Gore MA

Sorghum and maize share a close evolutionary history that can be explored through comparative genomics. To perform a large-scale comparison of the genomic variation between these two species, we analyzed 13M variants identified from whole genome resequencing (WGS) of 468 sorghum lines together with 25M variants previously identified in 1,218 maize lines. Deleterious mutations in both species were prevalent in pericentromeric regions, enriched in non-syntenic genes, and present at low allele frequencies. A comparison of deleterious burden between sorghum and maize revealed that sorghum, in contrast to maize, departed from the “domestication cost” hypothesis that predicts a higher deleterious burden among domesticates compared to wild lines. Additionally, sorghum and maize population genetic summary statistics were used to predict a gene deleterious index with an accuracy higher than 0.5. This research represents a key step towards understanding the evolutionary dynamics of deleterious variants in sorghum and provides a comparative genomics framework to start prioritizing them for removal through genome editing and breeding.

Other papers by lab members

Cathy Rushworth

Rushworth, C.A., and T. Mitchell-Olds. 2021. The evolution of sex is tempered by costly hybridization in Boechera (rock cress). Journal of Heredity 112(1): 67-77 https://doi.org/10.1093/jhered/esaa041.

Rushworth, C.A., R.S. Baucom, B.K. Blackman, M. Neiman, M.E. Orive, A. Sethuraman, J. Ware, and D.R. Matute. 2021. Who are we now? A demographic assessment of the evolution societies. Evolution 75(2): 208-218 https://onlinelibrary.wiley.com/doi/10.1111/evo.14168.

Carley, L.N., J.P. Mojica, B. Wang, C.-Y. Chen, Y.-P. Lin, K.V.S.K. Prasad, E. Chan, C.-W. Hsu, R. Keith, C.L. Nuñez, C.F. Olson-Manning, C.A. Rushworth, M.R. Wagner, J. Wang, P.-M. Yeh, M. Reichelt, K. Ghattas, J. Gershenzon, C.-R. Lee, and T. Mitchell-Olds. 2021. Ecological factors influence balancing selection on leaf chemical profiles of a wildflower. Nature Ecology and Evolution https://doi.org/10.1038/s41559-021-01486-0.

Mitra Menon

Menon, M., Bagley, J.C., Page, G.F.M. et al. Adaptive evolution in a conifer hybrid zone is driven by a mosaic of recently introgressed and background genetic variants. Commun Biol 4, 160 (2021). https://doi.org/10.1038/s42003-020-01632-7

Silas Tittes

O’Hara, N. B., Franks, S. J., Kane, N. C., Tittes, S., & Rest, J. S. (2021). Evolution of pathogen response genes associated with increased disease susceptibility during adaptation to an extreme drought in a Brassica rapa plant population. BMC Ecology and Evolution, 21(1), 1-11.  

2020

Adaptive evolution of DNA methylation reshaped gene regulation in maize [preprint] [github]
Xu G, Lyu J, Li Q, Liu H, Wang D, Zhang M, Springer NM, Ross-Ibarra J, Yang J

DNA methylation is a ubiquitous chromatin feature – in maize, more than 25% of cytosines in the genome are methylated. Recently, major progress has been made in describing the molecular mechanisms driving methylation, yet variation and evolution of the methylation landscape during maize domestication remain largely unknown. Here we leveraged whole-genome sequencing (WGS) and whole-genome bisulfite sequencing (WGBS) on populations of modern maize, landrace, and teosinte (Zea mays ssp. parviglumis) to investigate the adaptive and phenotypic consequences of methylation variations in maize. By using a novel estimation approach, we inferred the methylome site frequency spectrum (mSFS) to estimate forward and backward methylation mutation rates and selection coefficients. We only found weak evidence for direct selections on methylations in any context, but thousands of differentially methylated regions (DMRs) were identified in population-wide that are correlated with recent selections. Further investigation revealed that DMRs are enriched in 5’ untranslated regions, and that maize hypomethylated DMRs likely helped rewire distal gene regulation. For two trait-associated DMRs, vgt1-DMR and tb1-DMR, our HiChIP data indicated that the interactive loops between DMRs and respective downstream genes were present in B73, a modern maize line, but absent in teosinte. And functional analyses suggested that these DMRs likely served as cis-acting elements that modulated gene regulation after domestication. Our results enable a better understanding of the evolutionary forces acting on patterns of DNA methylation and suggest a role of methylation variation in adaptive evolution.

The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication
Chen Q, Fernando Samayoa L, Yang CJ, …[5 authors]… Lorant A, Buckler ES, Ross-Ibarra J, Holland JB, Doebley JF

The genetics of domestication has been extensively studied ever since the rediscovery of Mendel’s law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high F ST ) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is “missing” in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect.

Loss of diversity and accumulation of genetic load in doubled-haploid lines from European maize landraces [preprint][github]
Zeitler L, Ross-Ibarra J, Stetter MGS

Maize landraces are well adapted to their local environments and present valuable sources of genetic diversity for breeding and conservation. But the maintenance of open-pollinated landraces in programs is challenging, as regeneration of seed can often lead to inbreeding depression and the loss of diversity due to genetic drift. Recent reports suggest that the production of doubled-haploid (DH) lines from landraces may serve as a convenient means to preserve useful genetic diversity in a homozygous form that is immediately useful for modern breeding. The production of doubled-haploid (DH) lines presents an extreme case of inbreeding which results in instantaneous homozygosity genome-wide. Here we analyzed the effect of DH production on genetic diversity, using genome-wide SNP data from hundreds of individuals of five European landraces and their related DH lines. In contrast to previous findings, we observe a dramatic loss of diversity at both the haplotype level and that of individual SNPs. We identify thousands of SNPs that exhibit allele frequency differences larger than expected under models of neutral genetic drift, and document patterns of heterozygosity and polymorphism at conserved sites that suggest an important role for deleterious recessive load in determining diversity differences between landrace and DH populations. Although we were unable to uncover more details about the mode of selection, we conclude that while landrace DH lines may be a valuable tool for the introduction of variation into maize breeding programs they come at the cost of decreased genetic diversity and increased genetic load.

Genome-wide selection and genetic improvement during modern maize breeding
Wang B, Lin Z, Li X, Zhao Y …[17 authors]… Hufford MB, Ross-Ibarra J, He H, Wang H.

Modern crop breeding has made a profound impact on food production to sustain population growth during the past century; however, systematic analyses of the genomic basis underlying the dramatic increase in crop yields during modern breeding remain limited in scope. Here we report an analysis of the genomic and phenotypic changes associated with modern maize breeding across a chronological sampling of 350 elite inbred lines representing multiple eras of both Chinese and U.S. germplasm. We document a number of convergent phenotypic changes in both countries. Using genome-wide association and selection scan methods, we identify 160 loci underlying adaptive agronomic phenotypes and more than 1,800 genomic regions representing the targets of selection during modern breeding. We functionally validate two candidate genes underpinning variation in ear height and tassel branch number using CRISPR knockout mutants. In sum, this work demonstrates the utility of breeding-era approach for identifying breeding signatures and lays the foundation for future genomics-enabled maize breeding.”

Evolutionary insights into plant breeding [preprint]
Turner-Hissong SD, Mabry ME, Beissinger TM, Ross-Ibarra J, Pires JC

<p style="margin-left: 30px">Crop domestication is a fascinating area of study, as evidencedby a multitude of recent reviews. Coupled with the increasing availability of genomic and phenomic resources in numerous crop species, insights from evolutionary biology will enable a deeper understanding of the genetic architecture and short-term evolution of complex traits, which can be used to inform selection strategies. Future advances in crop improvement will rely on the integration of population genetics with  plant  breeding  methodology,  and  the  development  of  community  resources  to  support research in a variety of crop life histories and reproductive strategies. We highlight recent advances in the role of selective sweeps and demographic history in shaping genetic architecture, how these breakthroughs can inform selection strategies, and the application of precision gene editing to leverage these connections.

Genomics of long- and short- term adaptation in maize and teosinte [preprint]
Lorant A, Ross-Ibarra J, Tenaillon M

We review studies on short and long term adaptation, both natural and artificial, in maize and teosinte.

The temporal dynamics of background selection in non-equilibrium populations [preprint][github]
Torres R, Stetter MG, Hernandez R, Ross-Ibarra J

We use simulations to show that the effects of nonequilibrium population dynamics on linked selection differ qualitatively from predictions under equilibrium models, calling into question inferences about the efficacy of selection made from summary statistics.

Other papers by lab members

Catherine Rushworth

Rushworth, C.A., R.S. Baucom, B.K. Blackman, M. Neiman, M.E. Orive, A. Sethuraman, J. Ware, and D.R. Matute. 2021. Who are we now? A demographic assessment of the evolution societies. In press, Evolution. Early View: https://onlinelibrary.wiley.com/doi/10.1111/evo.14168.  

Rushworth, C.A., and T. Mitchell-Olds. 2021. The evolution of sex is tempered by costly hybridization in Boechera (rock cress). Journal of Heredity Early View: https://doi.org/10.1093/jhered/esaa041.  

Rushworth, C.A., Y. J. Brandvain, and T. Mitchell-Olds. 2020. Identifying the fitness consequences of sex in complex natural environments. Evolution Letters 4-6: 516-529. https://dx.doi.org/10.1002/evl3.194  

Jordon-Thaden, I., J. Beck, C.A. Rushworth, M.D. Windham, N. Diaz, J. Cantley, C. Martine, and C.J. Rothfels. 2020. RADseq for any lab: a basic two-enzyme protocol performs well in herbarium and silica-dried tissues across four genera. Applications in Plant Sciences 8(4): e11344.  

Silas Tittes

Tittes, Silas. "rdmc: an open source R package implementing convergent adaptation models of Lee and Coop (2017)." G3: Genes, Genomes, Genetics 10.9 (2020): 3041-3046.  

Wooliver, R., Tittes, S. B., & Sheth, S. N. (2020). A resurrection study reveals limited evolution of thermal performance in response to recent climate change across the geographic range of the scarlet monkeyflower. Evolution, 74(8), 1699-1710.  

Comeault, A. A., Wang, J., Tittes, S., Isbell, K., Ingley, S., Hurlbert, A. H., & Matute, D. R. (2020). Genetic diversity and thermal performance in invasive and native populations of African fig flies. Molecular biology and evolution, 37(7), 1893-1906.

2019

Single gene resolution of locally adaptive genetic variation in Mexican maize [preprint]
Gates DJ, Runcie D, Janzen GM, Romero Navarro A …[4 authors]… Buckler ES, Hearne S, Hufford MB, Ross-Ibarra J

We present a high-resolution genome-wide association analysis to identify loci exhibiting adaptive patterns in a large panel of more than 4500 traditional maize landraces representing the breadth of genetic diversity of maize in Mexico. We evaluate associations between genotype and plant performance in 13 common gardens across a range of environments, identifying hundreds of candidate genes underlying genotype by environment interaction. We further identify genetic associations with environment across Mexico and show that such loci are associated with variation in yield and flowering time in our field trials and predict performance in independent drought trials. Our results indicate that the variation necessary to adapt crops to changing climate exists in traditional landraces that have been subject to ongoing environmental adaptation and can be identified by both phenotypic and environmental association.

Dynamic patterns of transcript abundance of transposable element families in maize [preprint]
Anderson SN, Stitzer MC, Zhou P, Ross-Ibarra J, Hirsch CD, Springer NM

We develop an approach to estiamte family-level expression in transposable elements. While a relatively small proportion of TE families are transcribed, expression is highly dynamic with most families exhibiting tissue-specific expression. We also assay expression among different maize genotypes and use a mapping population to identify what proportion of copies in a family contribute to expression.”

Transposable elements contribute to dynamic genome content in maize [preprint]
Anderson SN*, Stitzer MC*, Brohammer AB*, Peng Zhou P, Noshay JM, Hirsch CD, Ross-Ibarra J, Hirsch CN, Springer NM

We identify hundreds of thousands of variable transposable elements among a small set of maize genome assemblies. We find evidence of a large number of genes impacted by TEs, including TEs in genes and genes in TEs, and evidence of recent transposition as well.””

Hybrid decay: a transgenerational epigenetic decline in vigor and viability triggered in backcross populations of teosinte with maize [preprint]
Wei X, Anderson SN, Wang X, …[Bilinski P, Stitzer MC, Ross-Ibarra J and 4 other authors]… Chen X, Springer NM, Doebley JF

We describe a phenomenon we name ‘hybrid decay’ triggered by backcrossing between domesticated maize and a specific teosinte population, resulting in genome instability, activation of transposable elements, and altered epigenetics .”

Adaptive phenotypic divergence in teosinte differs across biotic contexts [preprint] [perspective]
O’Brien AM, Sawers RJH, Strauss SY, Ross-Ibarra J

We show that rhizosphere biota impact adaptive divergence of phenotypic traits in teosinte along an environmental cline. This work suggests an important role for biotic interactions in determining the outcome of local adaptation.

Characterization of introgression from the teosinte Zea mays ssp. mexicana to Mexican highland maize [preprint]
Gonzalez-Segovia E, Pérez-Limon S, C Cíntora-Martínez C, Guerrero-Zavala A, Jansen G, Hufford MB, Ross-Ibarra J, Ruairidh J H Sawers

We look for introgression from teosinte in the genomes of two highland landraces and use QTL mapping to test for functional relevance of introgressed regions.

Detecting adaptive differentiation in structured populations with genomic data and common gardens [preprint] [github]
Josephs EB, Berg JJ, Ross-Ibarra J, Coop G

We develop methods to detect polygenic adaptation on phenotypes from common gardens and GWAS panels.

Other papers by lab members

Taylor Perkins

Perkins, M. Taylor, Tetyana Zhebentyayeva, Paul H. Sisco, and J. Hill Craddock. “Genome-wide sequence-based genotyping supports a nonhybrid origin of Castanea alabamensis.” bioRxiv (2019): 680371.   

Craddock, J. Hill, and M. Taylor Perkins. “Chestnut (Castanea spp. Miller) Breeding.” In Advances in Plant Breeding Strategies, vol. 4. (J.M. Al-Khayri et al., eds.)(in press), 55 pages. Springer Nature Switzerland AG, Basel.  

Michelle Stitzer

Roessler, Kyria, Aline Muyle, Concepcion M. Diez, Garren RJ Gaut, Alexandros Bousios, Michelle C. Stitzer, Danelle K. Seymour, John F. Doebley, Qingpo Liu, and Brandon S. Gaut. "The genome-wide dynamics of purging during selfing in maize." Nature plants (2019): 1-11.  

Noshay, Jaclyn M., Sarah N. Anderson, Peng Zhou, Lexiang Ji, William Ricci, Zefu Lu, Michelle C. Stitzer et al. "Monitoring the interplay between transposable element families and DNA methylation in maize." PLoS genetics 15, no. 9 (2019): e1008291.     

Marcela K. Tello-Ruiz, Cristina F. Marco, Fei-Man Hsu, Rajdeep S. Khangura, Pengfei Qiao, Sirjan Sapkota, Michelle C. Stitzer, Rachael Wasikowski, Hao Wu, Junpeng Zhan, Kapeel Chougule, Lindsay C. Barone, Cornel Ghiban, Demitri Muna, Andrew C. Olson, Liya C. Wang, Doreen C. Ware, David A. Micklos bioRxiv 654848; doi: https://doi.org/10.1101/654848  

Stitzer, Michelle C., and Philipp Brand. "Digest: Hybrid incompatibilities and introgression in wild monkeyflowers." Evolution 72, no. 11 (2018): 2565-2566.

2018

Genetic architecture and selective sweeps after polygenic adaptation to distant trait optima [preprint] [interactive]
Stetter MG, Thornton K, Ross-Ibarra J

We use simulations to study the population genetics of selection on a quantitative trait and learn which parameters drive quantitative trait evollution.

Evolutionary responses to conditionality in species interactions across environmental gradients [preprint][review]
O’Brien AM, Sawers RJH, Ross-Ibarra J, Strauss SY

We present the CoCoA hypothesis which describes how patterns of biotic coadpation change across varying abiotic environments

Evolution and Adaptation in the Maize Genome
Manchanda N, Snodgrass SJ, Ross-Ibarra J, Hufford MB

We review progress thus far in genomic research of maize domestication and adaptation. We discuss the insights genomics has shed on our understanding of these processes and conclude with a future outlook for how genomics might be further applied.

Maize domestication and gene interaction [preprint]
Stitzer MC, Ross-Ibarra J

We review genetic work looking at the role of dominance, epistasis, and pleiotropy during maize domestication.

A novel maize kinesin causes neocentromere activity and meiotic drive, altering inheritance patterns across the genome [pdf] [YouTube]
Dawe RK, Lowry EG, Gent JI, Stitzer MC, Higgins DM, Ross-Ibarra J, Wallace J, Kanizay LB … [7 authors]

We identify a small gene family Kindr as the causal locus for meiotic drive in maize.

Parallel altitudinal clines reveal adaptive evolution of genome size in Zea mays [perspective] [preprint] [github] [slides]
Bilinski P, Albert P, Berg JJ, Birchler JA, Grote M, Lorant A, Quezada J, Swarts K, Yang J, Ross-Ibarra J

We show that genome size can be analyzed as a quantitative trait and that selection on flowering time in maize has likely driven adaptive changes in genome size along multiple altitudinal clines.

Adaptation in plant genomes: bigger is different [preprint][github][YouTube][slides]
Mei W, Stetter MG, Gates DJ, Stitzer MC, Ross-Ibarra J

We develop the functional space hypothesis in which we posit that adaptation in large genomes uses more noncoding variation and is more likely to proceed via soft sweeps.

Harnessing cross-border resources to confront climate change
Aburto-Oropeza O …[Ross-Ibarra J and 85 authors in alphabetical order]… Taylor JE

Discusses the challenges of changing climates pose for society and the environment along the Mexican-US border.

Other papers by lab members

Wenbin Mei and Michelle Stitzer

Springer, Nathan M., et al. "The maize W22 genome provides a foundation for functional genomics and transposon biology." Nature genetics (2018): 1.

Markus Stetter

Joshi, Dinesh C., et al. "From zero to hero: the past, present and future of grain amaranth breeding." Theoretical and Applied Genetics (2018): 1-17.

Emily Josephs

Josephs, Emily B. "Determining the evolutionary forces shaping G× E." New Phytologist (2018).

Uzunović, Jasmina, et al. "Transposable elements are important contributors to standing variation in gene expression in Capsella grandiflora." bioRxiv (2018): 289173.

Anne Lorant

Kremling, Karl AG, et al. "Dysregulation of expression correlates with rare-allele burden and fitness loss in maize." Nature 555.7697 (2018): 520.

Daniel Gates

Gates, Daniel J., Diana Pilson, and Stacey D. Smith. "Filtering of target sequence capture individuals facilitates species tree construction in the plant subtribe Iochrominae (Solanaceae)." Molecular phylogenetics and evolution 123 (2018): 26-34.

Gates, Daniel J., et al. "A novel R3 MYB transcriptional repressor associated with the loss of floral pigmentation in Iochroma." New Phytologist 217.3 (2018): 1346-1356.  

Dianne Velasco

Riaz, Summaira, et al. "Genetic diversity analysis of cultivated and wild grapevine (Vitis vinifera L.) accessions around the Mediterranean basin and Central Asia." BMC plant biology 18.1 (2018): 137.

2017

Construction of the third generation Zea mays haplotype map [preprint] [sequence data] [genotype data] [alignment data] [code]
Bukowski R …[16 authors]… Ross-Ibarra J, Lorant A, Buffalo V, Romay MC, Buckler ES, Ware D, Lai J, Sun Q, Xu Y

We present a SNP dataset of 80M variants from a sample of 1200 maize and teosinte genomes.

The interplay of demography and selection during maize domestication and diffusion [preprint][github][YouTube]
Wang L, Beissinger TM, Lorant A, Ross-Ibarra C, Ross-Ibarra J, Hufford MB.

We show how population bottlenecks and gene flow have shaped patterns of genetic load across the maize genome and among populatons.

Incomplete dominance of deleterious alleles contribute substantially to trait variation and heterosis in maize [preprint] [github]
Yang J, Mezmouk S, Baumgarten A, Buckler ES, Guill KE, McMullen MD, Mumm RH, Ross-Ibarra J

We combine phenotypic data from crosses between multiple maize inbred lines and genome-wide characterization of deleterious alleles to show that a simple model of incomplete dominance may help explain hybrid vigor.

The potential role of genetic assimilation during maize domestication [preprint]
Lorant A, Pedersen, S, Holst I, Hufford MB, Winter K, Piperno D, Ross-Ibarra J

Gene expression data from maize and teosinte grown in mid-Holocene environments suggests that for some genes plastic changes in expression may have preceded genetic changes during domestication.

Allele specific expression analysis identifies regulatory variation associated with stress-related genes in the Mexican highland maize landrace Palomero Toluqueño [preprint]
Aguilar-Rangel MR, Chávez Montes RA, Gonzalez-Segovia E, Ross-Ibarra J, Simpson JK, Sawers RJH

Background Gene regulatory variation has been proposed to play an important role in the adaptation of plants to environmental stress. In the central highlands of Mexico, farmer selection has generated a unique group of maize landraces adapted to the challenges of the highland niche. In this study, gene expression in Mexican highland maize and a reference maize breeding line were compared to identify evidence of regulatory variation in stress-related genes. It was hypothesised that local adaptation in Mexican highland maize would be associated with a transcriptional signature observable even under benign conditions.

Methods Allele specific expression analysis was performed using the seedling-leaf transcriptome of an F1 individual generated from the cross between the highland adapted Mexican landrace Palomero Toluqueño and the reference line B73, grown under benign conditions. Results were compared with a published dataset describing the transcriptional response of B73 seedlings to cold, heat, salt and UV treatments.

Results A total of 2,386 genes were identified to show allele specific expression. Of these, 277 showed an expression difference between Palomero Toluqueño and B73 alleles under benign conditions that anticipated the response of B73 cold, heat, salt and/or UV treatments, and, as such, were considered to display a prior stress response. Prior stress response candidates included genes associated with plant hormone signaling and a number of transcription factors. Construction of a gene co-expression network revealed further signaling and stress-related genes to be among the potential targets of the transcription factors candidates.

Discussion Prior activation of responses may represent the best strategy when stresses are severe but predictable. Expression differences observed here between Palomero Toluqueño and B73 alleles indicate the presence of cis-acting regulatory variation linked to stress-related genes in Palomero Toluqueño. Considered alongside gene annotation and population data, allele specific expression analysis of plants grown under benign conditions provides an attractive strategy to identify functional variation potentially linked to local adaptation.

Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America
Swarts K, Gutaker RM …[Ross-Ibarra J and 14 authors in alphabetical order]… Krause J, Matson RG, Weigel D, Buckler ES, Burbano HA

By 4000 years ago, people had introduced maize to the southwestern United States; full agriculture was established quickly in the lowland deserts but delayed in the temperate highlands for 2000 years. We test if the earliest upland maize was adapted for early flowering, a characteristic of modern temperate maize. We sequenced fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the temperate Southwest. Indirectly validated genomic models predicted that Turkey Pen maize was marginally adapted with respect to flowering, as well as short, tillering, and segregating for yellow kernel color. Temperate adaptation drove modern population differentiation and was selected in situ from ancient standing variation. Validated prediction of polygenic traits improves our understanding of ancient phenotypes and the dynamics of environmental adaptation. Nature News [Phys.org] [Science Daily]

How to make a domesticate [preprint]
Stetter MG, Gates DJ, Mei W, Ross-Ibarra J

A perspective that seeks to predict what factors influence the success of domestication, how many genes contributed to the process, where these genes originated and the implications for de novo domestication.

Improved maize reference genome with single-molecule technologies [preprint] [github]
Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, …[18 authors]… Ross-Ibarra J, Dawe K, Hastie A, Rank DR, Ware D

We present a high-quality long-read reference genome of the maize inbred B73 and the first detailed annotation of retroelements in any grass species. [NSF research news] [UCD press release]

Gene fractionation and function in the ancient subgenomes of maize [preprint]
Renny-Byfield S, Rodgers-Melnick E, Ross-Ibarra J

The maize genome experienced an ancient whole genome duplication ∼10 MYA and the duplicate subgenomes have since experienced reciprocal gene loss such that many genes have returned to single-copy status. This process has not affected the subgenomes equally; reduced gene expression in one of the subgenomes mitigates the consequences of mutations and gene deletions and is thought to drive higher rates of fractionation. Here, we use published data to show that, in accordance with predictions of this model, paralogs with greater expression contribute more to phenotypic variation compared with their lowly expressed counterparts. Furthermore, paralogous genes in the least-fractionated subgenome account for a greater degree of phenotypic diversity than those resident on the more-fractionated subgenome. Intriguingly, analysis of singleton genes reveals this difference persists even after fractionation is complete. Additionally, we show that the two subgenomes of maize may differ in their epigenetic profiles.

Genomic abundance is not predictive of tandem repeat localization in grass genomes [preprint] [github]
Bilinski P, Han Y, Hufford MB, Lorant A, Zhang P, Estep MC, Jiang J, Ross-Ibarra J

Highly repetitive regions have historically posed a challenge when investigating sequence variation and content. High-throughput sequencing has enabled researchers to use whole-genome shotgun sequencing to estimate the abundance of repetitive sequence, and these methodologies have been recently applied to centromeres. Previous research has investigated variation in centromere repeats across eukaryotes, positing that the highest abundance tandem repeat in a genome is often the centromeric repeat. To test this assumption, we used shotgun sequencing and a bioinformatic pipeline to identify common tandem repeats across a number of grass species. We find that de novo assembly and subsequent abundance ranking of repeats can successfully identify tandem repeats with homology to known tandem repeats. Fluorescent in-situ hybridization shows that de novo assembly and ranking of repeats from non-model taxa identifies chromosome domains rich in tandem repeats both near pericentromeres and elsewhere in the genome.

Other papers by lab members

Dianne Velasco

Aradhya, Mallikarjuna, et al. "Genetic and ecological insights into glacial refugia of walnut (Juglans regia L.)." PloS one 12.10 (2017): e0185974.

Emily Josephs

Josephs, Emily B., et al. "The relationship between selection, network connectivity, and regulatory variation within a population of Capsella grandiflora." Genome biology and evolution 9.4 (2017): 1099-1109.

Josephs, Emily B., John R. Stinchcombe, and Stephen I. Wright. "What can genome‐wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits?." New Phytologist 214.1 (2017): 21-33.

Wenbin Mei

Mei, Wenbin, et al. "A comprehensive analysis of alternative splicing in paleopolyploid maize." Frontiers in plant science 8 (2017): 694.

Liu, Xiaoxian, et al. "Detecting alternatively spliced transcript isoforms from single‐molecule long‐read sequences without a reference genome." Molecular ecology resources 17.6 (2017): 1243-1256.

Gault, Christine M., et al. "Aberrant splicing in maize rough endosperm3 reveals a conserved role for U12 splicing in eukaryotic multicellular development." Proceedings of the National Academy of Sciences (2017): 201616173.

Feng, Guanqiao, et al. "Evolution of the 3R-MYB gene family in plants." Genome biology and evolution 9.4 (2017): 1013-1029.

Mei, Wenbin, et al. "Evolutionarily conserved alternative splicing across monocots." Genetics (2017): genetics-300189.

2016

Genome sequence of a 5310-year-old maize cob provides insights into the early stages of maize domestication
Ramos-Madrigal J, Smith BD, Moreno-Mayar JV, Gopalakrishnan S, Ross-Ibarra J, Gilbert MTP, Wales N

Genome sequence of a 5,000 year old maize cob reveals it was partially domesticated and helps identify the timing of adaptation during domestication.

Evolutionary genomics of peach and almond domestication [preprint]
Velasco D, Hough J, Aradhya M, Ross-Ibarra J

Resequencing data from a number of peach and almond varieties show differences in population size and mating system, but little evidence for convergent selection during domestication.

ANGSD-wrapper: utilities for analyzing next generation sequencing data [github] [preprint]
Durvasula A, Hoffman PJ, Kent TV, Liu C, Kono TJY, Morrell PL, Ross-Ibarra J

We provide a set of scripts and configuration files to facilitate easy popgen analysis of short-read sequencing data.

Recent demography drives changes in linked selection across the maize genome [github] [preprint]
Beissinger TM, Wang L, Crosby K, Durvasula A, Hufford MB, Ross-Ibarra J

We find little evidence for widespread hard sweeps in maize or teosinte and show that differences in demography during maize domestication and subsequent expansion have have changed the impacts of linked selection on surrounding diversity in the maize genome.

Maize diversity associated with social origin and environmental variation in southern Mexico [preprint]
Orozco-Ramírez Q, Santacruz-Varela A, Ross-Ibarra J, Brush S

While prevailing theories of crop evolution suggest that crop diversity and cultural diversity should be linked, empirical evidence for such a link remains inconclusive. In particular, few studies have investigated such patterns on a local scale. Here, we address this issue by examining the determinants of maize diversity in a local region of high cultural and biological richness in Southern Mexico. We collected maize samples from villages at low and middle elevations in two adjacent municipalities of differing ethnicity: Mixtec or Chatino. Although morphological traits show few patterns of population structure, we see clear genetic differentiation among villages, with municipality explaining a larger proportion of the differentiation than altitude. Consistent with an important role of social origin in patterning seed exchange, metapopulation model-based estimates of differentiation match the genetic data within village and ethnically distinct municipalities, but underestimate differentiation when all four villages are taken together. Our research provides insights about the importance of social origin in structuring maize diversity at the local scale.

High quality maize centromere 10 sequence reveals evidence of frequent recombination events
Wolfgruber TK, Nakashima MM …[5 authors]… Bilinski P, Dawe RK, Ross-Ibarra J, Birchler JA, Presting G

The ancestral centromeres of maize contain long stretches of the tandemly arranged CentC repeat. The abundance of tandem DNA repeats and centromeric retrotransposons (CR) has presented a significant challenge to completely assembling centromeres using traditional sequencing methods. Here, we report a nearly complete assembly of the 1.85 Mb maize centromere 10 from inbred B73 using PacBio technology and BACs from the reference genome project. The error rates estimated from overlapping BAC sequences are 7 × 10−6 and 5 × 10−5 for mismatches and indels, respectively. The number of gaps in the region covered by the reassembly was reduced from 140 in the reference genome to three. Three expressed genes are located between 92 and 477 kb from the inferred ancestral CentC cluster, which lies within the region of highest centromeric repeat density. The improved assembly increased the count of full-length CR from 5 to 55 and revealed a 22.7 kb segmental duplication that occurred approximately 121,000 years ago. Our analysis provides evidence of frequent recombination events in the form of partial retrotransposons, deletions within retrotransposons, chimeric retrotransposons, segmental duplications including higher order CentC repeats, a deleted CentC monomer, centromere-proximal inversions, and insertion of mitochondrial sequences. Double-strand DNA break (DSB) repair is the most plausible mechanism for these events and may be the major driver of centromere repeat evolution and diversity. In many cases examined here, DSB repair appears to be mediated by microhomology, suggesting that tandem repeats may have evolved to efficiently repair frequent DSBs in centromeres.

Other papers by lab members

Dianne Velasco

Migicovsky, Zoë, et al. "Genomic ancestry estimation quantifies use of wild species in grape breeding." BMC genomics 17.1 (2016): 478.

Emily Josephs

Josephs, Emily B., and Stephen I. Wright. "On the Trail of Linked Selection." PLoS genetics 12.8 (2016): e1006240.

Tim Beissinger

Morota, Gota, Timothy M. Beissinger, and Francisco Peñagaricano. "MeSH-informed enrichment analysis and MeSH-guided semantic similarity among functional terms and gene products in chicken." G3: Genes, Genomes, Genetics (2016): g3-116.

2015

The genomic impacts of drift and selection for hybrid performance in maize [preprint]
Gerke JP, Edwards JW, Guill KE, Ross-Ibarra J, McMullen MD

Although maize is naturally an outcrossing organism, modern breeding utilizes highly inbred lines in controlled crosses to produce hybrids. The U.S. Department of Agriculture’s reciprocal recurrent selection experiment between the Iowa Stiff Stalk Synthetic (BSSS) and the Iowa Corn Borer Synthetic No. 1 (BSCB1) populations represents one of the longest running experiments to understand the response to selection for hybrid performance. To investigate the genomic impact of this selection program, we genotyped the progenitor lines and >600 individuals across multiple cycles of selection using a genome-wide panel of ∼40,000 SNPs. We confirmed previous results showing a steady temporal decrease in genetic diversity within populations and a corresponding increase in differentiation between populations. Thanks to detailed historical information on experimental design, we were able to perform extensive simulations using founder haplotypes to replicate the experiment in the absence of selection. These simulations demonstrate that while most of the observed reduction in genetic diversity can be attributed to genetic drift, heterozygosity in each population has fallen more than expected. We then took advantage of our high-density genotype data to identify extensive regions of haplotype fixation and trace haplotype ancestry to single founder inbred lines. The vast majority of regions showing such evidence of selection differ between the two populations, providing evidence for the dominance model of heterosis. We discuss how this pattern is likely to occur during selection for hybrid performance and how it poses challenges for dissecting the impacts of modern breeding and selection on the maize genome.

Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport [pdf]
Sosso D, Luo D, Li Q-B, Sasse J, Yang J …[6 authors]… Ross-Ibarra J, Yang B, Frommer WB

Carbohydrate import into seeds directly determines seed size and must have been increased through domestication. However, evidence of the domestication of sugar translocation and the identities of seed-filling transporters have been elusive. Maize ZmSWEET4c, as opposed to its sucrose-transporting homologs, mediates transepithelial hexose transport across the basal endosperm transfer layer (BETL), the entry point of nutrients into the seed, and shows signatures indicative of selection during domestication. Mutants of both maize ZmSWEET4c and its rice ortholog OsSWEET4 are defective in seed filling, indicating that a lack of hexose transport at the BETL impairs further transfer of sugars imported from the maternal phloem. In both maize and rice, SWEET4 was likely recruited during domestication to enhance sugar import into the endosperm.

Independent molecular basis of convergent highland adaptation in maize [preprint] [github] [data]
Takuno S, Ralph P, Swarts K, Elshire RJ, Glaubitz JC, Buckler ES, Hufford MB, Ross-Ibarra J

We find that maize adaptation to the highlands in Mexico and South America is largely independent and has made considerable use of standing genetic variation.

Natural variation in teosinte at the domestication locus teosinte branched1 (tb1) [preprint]
Vann LE, Kono TJ, Pyhäjärvi T, Hufford MB, Ross-Ibarra J.

We find that variation in the domestication locus tb1 does not explain a substantial proportion of phenotypic variation for tillering in natural populations of teosinte.

Genetic, evolutionary and plant breeding insights from the domestication of maize
Hake S, Ross-Ibarra J

The natural history of maize began nine thousand years ago when Mexican farmers started to collect the seeds of the wild grass, teosinte. Invaluable as a food source, maize permeated Mexican culture and religion. Its domestication eventually led to its adoption as a model organism, aided in large part by its large chromosomes, ease of pollination and growing agricultural importance. Genome comparisons between varieties of maize, teosinte and other grasses are beginning to identify the genes responsible for the domestication of modern maize and are also providing ideas for the breeding of more hardy varieties.

The origin and evolution of maize in the American Southwest [preprint] [data]
Fonseca RR, Smith B, Wales N, Cappellini E …[12 authors]… Hufford MB, Albrechtsen A, Ross-Ibarra J, Gilbert MT

We use sequence data from ancient maize cobs to reveal the timing and geography of maize introduction into the Southwest US. One of the most read papers from the last four years of the journal! UC Davis Press Release Science World Report Archaeology SiNC, Science magazine Nature Plants commentary The Scientist

Reply to Brush et al.: Wake-up call for crop conservation science
Dyer GA, Lopez-Feldman A, Yunez-Naude A, Taylor JE, Ross-Ibarra J

A response to Brush et al 2014

Transposable Elements Contribute to Activation of Maize Genes in Response to Abiotic Stress [preprint]
Makarevitch I, Waters M, West P, Stitzer M, Ross-Ibarra J, Springer NM

We show that transposable elements can act as regulatory sequences that up- or down-regulate genes in maize in response to abiotic stress.

Other papers by lab members

Dianne Velasco

Aradhya, Mallikarjuna, J. E. Preece, and Dianne Velasco. "Multivariate analysis of molecular and morphological diversity in fig (Ficus carica L.)." V International Symposium on Fig 1173. 2015.

Paul Bilinski

Leung, Wilson, et al. "Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution." G3: Genes, Genomes, Genetics 5.5 (2015): 719-740.

Anna O’Brien

Persson, Tomas, et al. "Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant." PLoS One 10.5 (2015): e0127630.

Shohei Takuno

Le, Tu N., et al. "Epigenetic regulation of intragenic transposable elements impacts gene transcription in Arabidopsis thaliana." Nucleic acids research 43.8 (2015): 3911-3921.

2014

Advances and limits of using population genetics to understand local adaptation [preprint] [correction]
Tiffin P, Ross-Ibarra J

We discuss some of the outstanding questions and key challenges facing the use of population genetics to study local adaptation.

Diversity and evolution of centromere repeats in the maize genome [preprint]
Bilinski P, Distor KD, Gutierez-Lopez J, Mendoza Mendoza G, Shi J, Dawe K, Ross-Ibarra J

Centromere repeats are found in most eukaryotes and play a critical role in kinetochore formation. Though centromere repeats exhibit considerable diversity both within and among species, little is understood about the mechanisms that drive centromere repeat evolution. Here, we use maize as a model to investigate how a complex history involving polyploidy, fractionation, and recent domestication has im- pacted the diversity of the maize centromeric repeat CentC. We first validate the existence of long tandem arrays of repeats in maize and other taxa in the genus Zea. Although we find considerable sequence diversity among CentC copies genome-wide, genetic similarity among repeats is highest within these arrays, suggesting that tandem du- plications are the primary mechanism for the generation of new copies. Nonetheless, clustering analyses identify similar sequences among distant repeats, and simulations suggest that this pattern may be due to homoplasious mutation. Although the two ancestral subgenomes of maize have contributed nearly equal numbers of centro- meres, our analysis shows that the majority of all CentC repeats derive from one of the parental genomes, with an even stronger bias when examining the largest as- sembled contiguous clusters. Finally, by comparing maize with its wild progenitor teosinte, we find that the abundance of CentC likely decreased after domesti- cation, while the pericentromeric repeat Cent4 has drastically increased.

The pattern and distribution of deleterious mutations in maize [preprint] [github]
Mezmouk S, Ross-Ibarra J

We show that deleterious mutations are abundant in modern maize breeding material and that genes with deleterious mutations are likely important contributors to phenotypic variation.

Other papers by lab members

2013

Comprehensive analysis of imprinted genes in maize reveals allelic variation and limited conservation with other species [preprint] [github]
Waters AJ, Bilinski P, Eichten SR, Vaugh MW, Ross-Ibarra J, Gehring M, Springer NM

In plants, a subset of genes exhibit imprinting in endosperm tissue such that expression is primarily from the maternal or paternal allele. Imprinting may arise as a consequence of mechanisms for silencing of transposons during reproduction, and in some cases imprinted expression of particular genes may provide a selective advantage such that it is conserved across species. Separate mechanisms for the origin of imprinted expression patterns and maintenance of these patterns may result in substantial variation in the targets of imprinting in different species. Here we present deep sequencing of RNAs isolated from reciprocal crosses of four diverse maize genotypes, providing a comprehensive analysis that allows evaluation of imprinting at more than 95% of endosperm-expressed genes. We find that over 500 genes exhibit statistically significant parent-of-origin effects in maize endosperm tissue, but focused our analyses on a subset of these genes that had >90% expression from the maternal allele (69 genes) or from the paternal allele (108 genes) in at least one reciprocal cross. Over 10% of imprinted genes show evidence of allelic variation for imprinting. A comparison of imprinting in maize and rice reveals that 13% of genes with syntenic orthologs in both species exhibit conserved imprinting. Genes that exhibit conserved imprinting between maize and rice have elevated nonsynonymous to synonymous substitution ratios compared with other imprinted genes, suggesting a history of more rapid evolution. Together, these data suggest that imprinting only has functional relevance at a subset of loci that currently exhibit imprinting in maize.

Complex patterns of local adaptation in teosinte [data] [preprint]
Pyhäjärvi T, Hufford MB, Mezmouk S, Ross-Ibarra J

Populations of widely distributed species encounter and must adapt to local environmental conditions. However, comprehensive characterization of the genetic basis of adaptation is demanding, requiring genome-wide genotype data, multiple sampled populations, and an understanding of population structure and potential selection pressures. Here, we used single-nucleotide polymorphism genotyping and data on numerous environmental variables to describe the genetic basis of local adaptation in 21 populations of teosinte, the wild ancestor of maize. We found complex hierarchical genetic structure created by altitude, dispersal events, and admixture among subspecies, which complicated identification of locally beneficial alleles. Patterns of linkage disequilibrium revealed four large putative inversion polymorphisms showing clinal patterns of frequency. Population differentiation and environmental correlations suggest that both inversions and intergenic polymorphisms are involved in local adaptation.

From many, one: genetic control of prolificacy during maize domestication [data] [preprint]
Wills DM, Whipple C, Takuno S, Kursel LE, Shannon LM, Ross-Ibarra J, Doebley JF.

A reduction in number and an increase in size of inflorescences is a common aspect of plant domestication. When maize was domesticated from teosinte, the number and arrangement of ears changed dramatically. Teosinte has long lateral branches that bear multiple small ears at their nodes and tassels at their tips. Maize has much shorter lateral branches that are tipped by a single large ear with no additional ears at the branch nodes. To investigate the genetic basis of this difference in prolificacy (the number of ears on a plant), we performed a genome-wide QTL scan. A large effect QTL for prolificacy (prol1.1) was detected on the short arm of chromosome 1 in a location that has previously been shown to influence multiple domestication traits. We fine-mapped prol1.1 to a 2.7 kb “causative region” upstream of the grassy tillers1 (gt1) gene, which encodes a homeodomain leucine zipper transcription factor. Tissue in situ hybridizations reveal that the maize allele of prol1.1 is associated with up-regulation of gt1 expression in the nodal plexus. Given that maize does not initiate secondary ear buds, the expression of gt1 in the nodal plexus in maize may suppress their initiation. Population genetic analyses indicate positive selection on the maize allele of prol1.1, causing a partial sweep that fixed the maize allele throughout most of domesticated maize. This work shows how a subtle cis-regulatory change in tissue specific gene expression altered plant architecture in a way that improved the harvestability of maize.

Agriculture: Feeding the future
McCouch S, Baute GJ, Bradeen J, Bramel P …[36 authors]… Ward J, Waugh R, Wenzl P, Zamir.

We must mine the biodiversity in seed banks to help to overcome food shortages, urge Susan McCouch and colleagues.

The genomic signature of crop-wild introgression in maize [data] [preprint]
Hufford MB, Lubinsky P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J

The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Population genetics and ethnobotany of cultivated Diospyros riojae (Ebenaceae), an endangered fruit crop from Mexico [preprint]
Provance MC, Garcia Ruiz I, Thommes C, Ross-Ibarra J

The traditional cultivation of an endan- gered species, Diospyros riojae, in North-Central Mexico, and the sale of its fruit, is described for the first time. This is complemented by the first examina- tion of genetic structure in New World Ebenaceae. Genetic comparisons are made among 27 accessions of D. riojae from across its known range of cultivation, and individuals of Diospyros conzattii, Diospyros digyna, Diospyros californica, Diospyros rosei, Diospyros rekoi and an unknown species of Diospyros from Oaxaca, Mexico. Morphological comparisons are made between D. conzattii, D. riojae, and the unknown species of Diospyros from Oaxaca. D. riojae is cultivated in two markedly different climates: arid and semi-arid localities west of the Sierra Gorda, especially near Tecozautla, Hidalgo, and humid areas of the Huasteca Region, east of the Sierra Gorda. Much lower levels of genetic diversity were detected in western populations, where populations are larger, and management intensity is the greatest. Neither the results of our genetic analysis, nor our morphological analysis of recent collections of D. riojae, D. conzattii, and an unknown species from Oaxaca, are consistent with the most recent revision of Neotropical Diospy- ros. Taxon-level divergence, rather than cultivar-level divergence, is suggested for D. riojae and D. conzattii.

Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution [preprint]
Melters DP, Bradnam KR, Young HA, Telis N …[9 authors]… Tobias C, Ross-Ibarra J, Korf IF, Chan SW-L.

Background
Centromeres are essential for chromosome segregation, yet their DNA sequences evolve rapidly. In most animals and plants that have been studied, centromeres contain megabase-scale arrays of tandem repeats. Despite their importance, very little is known about the degree to which centromere tandem repeats share common properties between different species across different phyla. We used bioinformatic methods to identify high-copy tandem repeats from 282 species using publicly available genomic sequence and our own data.

Results Our methods are compatible with all current sequencing technologies. Long Pacific Biosciences sequence reads allowed us to find tandem repeat monomers up to 1,419 bp. We assumed that the most abundant tandem repeat is the centromere DNA, which was true for most species whose centromeres have been previously characterized, suggesting this is a general property of genomes. High-copy centromere tandem repeats were found in almost all animal and plant genomes, but repeat monomers were highly variable in sequence composition and length. Furthermore, phylogenetic analysis of sequence homology showed little evidence of sequence conservation beyond approximately 50 million years of divergence. We find that despite an overall lack of sequence conservation, centromere tandem repeats from diverse species showed similar modes of evolution.

Conclusions While centromere position in most eukaryotes is epigenetically determined, our results indicate that tandem repeats are highly prevalent at centromeres of both animal and plant genomes. This suggests a functional role for such repeats, perhaps in promoting concerted evolution of centromere DNA across chromosomes.

Diversity and abundance of the Abnormal chromosome 10 meiotic drive complex in Zea mays [preprint]
Kanizay LB, Pyhäjärvi T, Lowry E, Hufford MB, Peterson DG, Ross-Ibarra J, Dawe RK

Maize Abnormal chromosome 10 (Ab10) contains a classic meiotic drive system that exploits the asymmetry of meiosis to preferentially transmit itself and other chromosomes containing specialized heterochromatic regions called knobs. The structure and diversity of the Ab10 meiotic drive haplotype is poorly understood. We developed a bacterial artificial chromosome (BAC) library from an Ab10 line and used the data to develop sequence-based markers, focusing on the proximal portion of the haplotype that shows partial homology to normal chromosome 10. These molecular and additional cytological data demonstrate that two previously identified Ab10 variants (Ab10-I and Ab10-II) share a common origin. Dominant PCR markers were used with fluorescence in situ hybridization to assay 160 diverse teosinte and maize landrace populations from across the Americas, resulting in the identification of a previously unknown but prevalent form of Ab10 (Ab10-III). We find that Ab10 occurs in at least 75% of teosinte populations at a mean frequency of 15%. Ab10 was also found in 13% of the maize landraces, but does not appear to be fixed in any wild or cultivated population. Quantitative analyses suggest that the abundance and distribution of Ab10 is governed by a complex combination of intrinsic fitness effects as well as extrinsic environmental variability.

Other papers by lab members

Dianne Velasco

Aradhya, Mallikarjuna, et al. "Genetic diversity, structure, and patterns of differentiation in the genus Vitis." Plant systematics and evolution 299.2 (2013): 317-330.

Zdunić, Goran, et al. "Genetic diversity and differentiation within and between cultivated (Vitis vinifera L. ssp. sativa) and wild (Vitis vinifera L. ssp. sylvestris) grapes." Vitis 52.1 (2013): 29-32.

2012

Teosinte as a model system for population and ecological genomics
Hufford MB, Bilinski P, Pyhäjärvi T, Ross-Ibarra J

As the cost of next-generation sequencing diminishes and genomic resources improve, crop wild relatives are well positioned to make major contributions to the field of ecological genomics via full-genome resequencing and reference-assisted de novo assembly of genomes of plants from natural populations. The wild relatives of maize, collectively known as teosinte, are a more varied and representative study system than many other model flowering plants. In this review of the population and ecological genomics of the teosintes we highlight recent advances in the study of maize domestication, introgres- sive hybridization, and local adaptation, and discuss future prospects for applying the genomic resources of maize to this intriguing group of species. The maize/ teosinte study system is an excellent example of how crops and their wild relatives can bridge the model/ non-model gap.

Comparative population genomics of maize domestication and improvement [data]
Hufford MB*, Xun X*, van Heerwaarden J*, Pyhäjärvi T* …[17 authors]… Ware D, Buckler ES, Yang S, Ross-Ibarra J

Domestication and plant breeding are ongoing 10,000-year- old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution1,2, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines3. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes4,5. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.

Using nextgen sequencing to investigate genome size variation and transposable element content
Munoz Diez C, Vitte C, Ross-Ibarra J, Gaut BS, Tenaillon MI

Transposable element (TE) content explains a large part of Eukaryotic genome size variation. TE content is determined by transposition, removal and host responses, but the efficiency of these forces is ultimately governed by genetic drift and natural selection. Contribution of TE families to genome size variation has been recently quantified using next generation sequencing (NGS) in two species pairs: Zea mays ssp. mays and Zea luxurians, Arabidopsis lyrata and A. thaliana. In both interspecific comparisons, genome-wide differences in TE content rather than the proliferation of a small subset of TE families was observed. We discuss three nonexclusive hypotheses to explain this pattern: selection for genome shrinkage, differential efficiency of epigenetic control, and a purely stochastic process of genome size evolution. Additional genome-wide assessments are needed to assess the extent to which selection shapes TE genomic content. To facilitate such studies, we discuss the use of NGS in “orphan” species.

Historical genomics of North American maize [data]
van Heerwaarden J, Hufford MB, Ross-Ibarra J

Since the advent of modern plant breeding in the 1930s, North American maize has undergone a dramatic adaptation to high-in- put agriculture. Despite the importance of genetic contributions to historical yield increases, little is known about the underlying ge- nomic changes. Here we use high-density SNP genotyping to char- acterize a set of North American maize lines spanning the history of modern breeding. We provide a unique analysis of genome- wide developments in genetic diversity, ancestry, and selection. The genomic history of maize is marked by a steady increase in genetic differentiation and linkage disequilibrium, whereas allele frequencies in the total population have remained relatively con- stant. These changes are associated with increasing genetic sepa- ration of breeding pools and decreased diversity in the ancestry of individual lines. We confirm that modern heterotic groups are the product of ongoing divergence from a relatively homogeneous landrace population, but show that differential landrace ancestry remains evident. Using a recent association approach, we charac- terize signals of directional selection throughout the genome, identifying a number of candidate genes of potential agronomic relevance. However, overall we find that selection has had limited impact on genome-wide patterns of diversity and ancestry, with little evidence for individual lines contributing disproportionately to the accumulation of favorable alleles in today’s elite germ- plasm. Our data suggest breeding progress has mainly involved selection and recombination of relatively common alleles, contrib- uted by a representative but limited set of ancestral lines.

Reshaping of the maize transcriptome by domestication
Swanson-Wagner R, Briskine R, Schaefer R, Hufford MB, Ross-Ibarra J, Myers CL, Tiffin P, Springer NM

Through domestication, humans have substantially altered the morphology of Zea mays ssp. parviglumis (teosinte) into the cur- rently recognizable maize. This system serves as a model for study- ing adaptation, genome evolution, and the genetics and evolution of complex traits. To examine how domestication has reshaped the transcriptome of maize seedlings, we used expression profil- ing of 18,242 genes for 38 diverse maize genotypes and 24 teo- sinte genotypes. We detected evidence for more than 600 genes having significantly different expression levels in maize compared with teosinte. Moreover, more than 1,100 genes showed signifi- cantly altered coexpression profiles, reflective of substantial rewir- ing of the transcriptome since domestication. The genes with altered expression show a significant enrichment for genes pre- viously identified through population genetic analyses as likely targets of selection during maize domestication and improvement; 46 genes previously identified as putative targets of selection also exhibit altered expression levels and coexpression relationships. We also identified 45 genes with altered, primarily higher, expres- sion in inbred relative to outcrossed teosinte. These genes are enriched for functions related to biotic stress and may reflect responses to the effects of inbreeding. This study not only docu- ments alterations in the maize transcriptome following domesti- cation, identifying several genes that may have contributed to the evolution of maize, but highlights the complementary information that can be gained by combining gene expression with population genetic analyses.

Maize HapMap2 identifies extant variation from a genome in flux
Chia J-M, Song C, …[Hufford, MB, Pyhäjärvi T, and 27 authors]… Ross-Ibarra, J, McMullen MD, Buckler ES, Zhang G, Xu Y, Ware, D

Whereas breeders have exploited diversity in maize for yield improvements, there has been limited progress in using beneficial alleles in undomesticated varieties. Characterizing standing variation in this complex genome has been challenging, with only a small fraction of it described to date. Using a population genetics scoring model, we identified 55 million SNPs in 103 lines across pre-domestication and domesticated Zea mays varieties, including a representative from the sister genus Tripsacum. We find that structural variations are pervasive in the Z. mays genome and are enriched at loci associated with important traits. By investigating the drivers of genome size variation, we find that the larger Tripsacum genome can be explained by transposable element abundance rather than an allopolyploid origin. In contrast, intraspecies genome size variation seems to be controlled by chromosomal knob content. There is tremendous overlap in key gene content in maize and Tripsacum, suggesting that adaptations from Tripsacum (for example, perennialism and frost and drought tolerance) can likely be integrated into maize.

Megabase-scale inversion polymorphism in the wild ancestor of maize [data]
Fang Z, Pyhäjärvi T, Weber AL, Dawe RK, …[2 authors]… Ross-Ibarra C, Doebley J, Morrell PL, Ross-Ibarra J

We identify and study the evolutionary genetics of a 50Mb inversion in natural populations of teosinte

Genetic architecture of maize kernel composition in the Nested Association Mapping and Inbred Association panels
Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, Ross-Ibarra J, Buckler ES, Flint-Garcia SA

The maize (Zea mays) kernel plays a critical role in feeding humans and livestock around the world and in a wide array of industrial applications. An understanding of the regulation of kernel starch, protein, and oil is needed in order to manipulate composition to meet future needs. We conducted joint-linkage quantitative trait locus mapping and genome-wide association studies (GWAS) for kernel starch, protein, and oil in the maize nested association mapping population, composed of 25 recombinant inbred line families derived from diverse inbred lines. Joint-linkage mapping revealed that the genetic architecture of kernel composition traits is controlled by 21–26 quantitative trait loci. Numerous GWAS associations were detected, including several oil and starch associations in acyl-CoA:diacylglycerol acyltransferase1-2, a gene that regulates oil composition and quantity. Results from nested association mapping were verified in a 282 inbred association panel using both GWAS and candidate gene association approaches. We identified many beneficial alleles that will be useful for improving kernel starch, protein, and oil content.

Crop genomics: advances and applications
Morrell PL, Buckler ES, Ross-Ibarra J

The completion of reference genome sequences for many important crops and the ability to perform high-throughput resequencing are providing opportunities for improving our understanding of the history of plant domestication and to accelerate crop improvement. Crop plant comparative genomics is being transformed by these data and a new generation of experimental and computational approaches. The future of crop improvement will be centred on comparisons of individual plant genomes, and some of the best opportunities may lie in using combinations of new genetic mapping strategies and evolutionary analyses to direct and optimize the discovery and use of genetic variation. Here we review such strategies and insights that are emerging.

Other papers by lab members

Tanja Pyhäjärvi

Krutovsky, Konstantin V., et al. "Gene flow, spatial structure, local adaptation, and assisted migration in trees." Genomics of tree crops. Springer, New York, NY, 2012. 71-116.

Pyhäjärvi, Tanja, Esa Aalto, and Outi Savolainen. "Time scales of divergence and speciation among natural populations and subspecies of Arabidopsis lyrata (Brassicaceae)." American journal of botany 99.8 (2012): 1314-1322.

Matthew Hufford

Hufford, Matthew B., et al. "Inferences from the historical distribution of wild and domesticated maize provide ecological and evolutionary insight." PLoS One 7.11 (2012): e47659.

2011

Identification of a functional transposon insertion in the maize domestication gene tb1 [data]
Studer A, Zhao Q, Ross-Ibarra J, Doebley J

Genetic diversity created by transposable elements is an important source of functional variation upon which selection acts during evolution1–6. Transposable elements are associated with adaptation to temperate climates in Drosophila7, a SINE element is associated with the domestication of small dog breeds from the gray wolf8 and there is evidence that transposable elements were targets of selection during human evolution9. Although the list of examples of transposable elements associated with host gene function continues to grow, proof that transposable elements are causative and not just correlated with functional variation is limited. Here we show that a transposable element (Hopscotch) inserted in a regulatory region of the maize domestication gene, teosinte branched1 (tb1), acts as an enhancer of gene expression and partially explains the increased apical dominance in maize compared to its progenitor, teosinte. Molecular dating indicates that the Hopscotch insertion predates maize domestication by at least 10,000 years, indicating that selection acted on standing variation rather than new mutation.

Genetic signals of origin, spread and introgression in a large sample of maize landraces [data]
van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM, Sanchez Gonzalez JJ, Ross-Ibarra J

We resolve the conflict between genetic, ecological, and achaeological data regarding the geographic location of maize domestication.

Influence of cryptic population structure on observed mating patterns in the wild progenitor of maize [data]
Hufford MB, Gepts P, Ross-Ibarra J

Indirect two-generation analysis of pollen flow has proven to be an effective alternative to exhaustive paternity analysis in numerous plant populations. In this investigation, the method is extended to an annual wild maize species, Zea mays ssp. parviglumis (Poaceae). Our analysis of mating system in parviglumis revealed high levels of outcrossing and higher biparental inbreeding than typically observed in grasses. Pollen dispersal analysis suggested low levels of long-distance dispersal. Given previous evidence for intrapopulation genetic structure in parviglumis populations, we explored the impact of cryptic population structure on estimates of mating system and pollen flow. Subpopulations inferred through spatially explicit Bayesian assignment showed mark- edly different values for both mating system parameters and pollen flow than the entire population. Finally, a novel method of pollen haplotype assignment revealed nonrandom mating consistent with intrapopulation structure. These results indicate parviglumis could be particularly susceptible to habitat fragmentation currently occurring throughout Mexico due to recent changes in land use.

Genome size and TE content as determined by high-throughput sequencing in maize and Zea luxurians
Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J

The genome of maize (Zea mays ssp. mays) consists mostly of transposable elements (TEs) and varies in size among lines. This variation extends to other species in the genus Zea: although maize and Zea luxurians diverged only ∼140,000 years ago, their genomes differ in size by ∼50%. We used paired-end Illumina sequencing to evaluate the potential contribution of TEs to the genome size difference between these two species. We aligned the reads both to a filtered gene set and to an exemplar database of unique repeats representing 1,514 TE families; ∼85% of reads mapped against TE repeats in both species. The relative contribution of TE families to the B73 genome was highly correlated with previous estimates, suggesting that reliable estimates of TE content can be obtained from short high-throughput sequencing reads, even at low coverage. Because we used paired-end reads, we could assess whether a TE was near a gene by determining if one paired read mapped to a TE and the second read mapped to a gene. Using this method, Class 2 DNA elements were found significantly more often in genic regions than Class 1 RNA elements, but Class 1 elements were found more often near other TEs. Overall, we found that both Class 1 and 2 TE families account for ∼70% of the genome size difference between B73 and luxurians. Interestingly, the relative abundance of TE families was conserved between species (r = 0.97), suggesting genome-wide control of TE content rather than family-specific effects.

Other papers by lab members

Tanja Pyhäjärvi

Savolainen, Outi, et al. "Adaptive potential of northernmost tree populations to climate change, with emphasis on Scots pine (Pinus sylvestris L.)." Journal of Heredity 102.5 (2011): 526-536.

Pyhäjärvi, Tanja, Sonja T. Kujala, and Outi Savolainen. "Revisiting protein heterozygosity in plants—nucleotide diversity in allozyme coding genes of conifer Pinus sylvestris." Tree genetics & genomes 7.2 (2011): 385-397.

2010

Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda)
Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonzalez-Martinez SC, and Neale DB

Natural populations of forest trees exhibit striking phenotypic adaptations to diverse environmental gradients, thereby making them appealing subjects for the study of genes underlying ecologically relevant phenotypes. Here, we use a genome-wide data set of single nucleotide polymorphisms genotyped across 3059 functional genes to study patterns of population structure and identify loci associated with aridity across the natural range of loblolly pine (Pinus taeda L.). Overall patterns of population structure, as inferred using principal components and Bayesian cluster analyses, were consistent with three genetic clusters likely resulting from expansions out of Pleistocene refugia located in Mexico and Florida. A novel application of association analysis, which removes the confounding effects of shared ancestry on correlations between genetic and environmental variation, identified five loci correlated with aridity. These loci were primarily involved with abiotic stress response to temperature and drought. A unique set of 24 loci was identified as FST outliers on the basis of the genetic clusters identified previously and after accounting for expansions out of Pleistocene refugia. These loci were involved with a diversity of physiological processes. Identification of nonoverlapping sets of loci highlights the fundamental differences implicit in the use of either method and suggests a pluralistic, yet complementary, approach to the identification of genes underlying ecologically relevant phenotypes.

Reproductive biology of Macleania rupestris (Ericaceae): a pollen-limited Neotropical cloud-forest species in Costa Rica
Fuchs EJ, Ross-Ibarra J, Barrantes G

A role for nonadaptive processes in plant genome size evolution?
Whitney KD, Baack EJ, Hamrick JL, Godt, MJW …[3 authors]… Goodwillie C, Kalisz S, Leitch I, Ross-Ibarra J

Genome sizes vary widely among species, but comprehensive explanations for the emergence of this variation have not been validated. Lynch and Conery (2003) hypothesized that genome expansion is maladaptive, and that lineages with small effective population size (Ne) evolve larger genomes than those with large Ne as a consequence of the lowered efficacy of natural selection in small populations. In addition, mating systems likely affect genome size evolution via effects on both Ne and the spread of transposable elements (TEs). We present a comparative analysis of the effects of Ne and mating system on genome size evolution in seed plants. The dataset includes 205 species with monoploid genome size estimates (corrected for recent polyploidy) ranging from 2Cx = 0.3 to 65.9 pg. The raw data exhibited a strong positive relationship between outcrossing and genome size, a negative relationship between Ne and genome size, but no detectable Ne × outcrossing interaction. In contrast, phylogenetically independent contrast analyses found only a weak relationship between outcrossing and genome size and no relationship between Ne and genome size. Thus, seed plants do not support the Lynch and Conery mechanism of genome size evolution. Further work is needed to disentangle contrasting effects of mating systems on the efficacy of selection and TE transmission.

Fine scale genetic structure in the wild ancestor of maize (Zea mays ssp. parviglumis)
van Heerwaarden J, Ross-Ibarra J, Doebley J, Glaubitz JC, Sanchez Gonzalez J, Gaut BS, Eguiarte LE

Analysis of fine scale genetic structure in continuous populations of outcrossing plant species has traditionally been limited by the availability of sufficient markers. We used a set of 468 SNPs to characterize fine-scale genetic structure within and between two dense stands of the wild ancestor of maize, teosinte (Zea mays ssp. parviglumis). Our analyses confirmed that teosinte is highly outcrossing and showed little population structure over short distances. We found that the two populations were clearly genetically differen- tiated, although the actual level of differentiation was low. Spatial autocorrelation of relatedness was observed within both sites but was somewhat stronger in one of the populations. Using principal component analysis, we found evidence for significant local differentiation in the population with stronger spatial autocorrelation. This differentiation was associated with pronounced shifts in the first two principal components along the field. These shifts corresponded to changes in allele frequencies, potentially due to local topographical features. There was little evidence for selection at individual loci as a contributing factor to differentiation. Our results demonstrate that significant local differentiation may, but need not, co-occur with spatial autocorrelation of relatedness. The present study represents one of the most detailed analyses of local genetic structure to date and provides a benchmark for future studies dealing with fine scale patterns of genetic diversity in natural plant populations.

Widespread gene conversion in centromere cores
Shi J, Wolf S, Burke J, Presting G, Ross-Ibarra J, Dawe RK

Centromeres are the most dynamic regions of the genome, yet they are typified by little or no crossing over, making it difficult to explain the origin of this diversity. To address this question, we developed a novel CENH3 ChIP display method that maps kinetochore footprints over transposon-rich areas of centromere cores. A high level of polymorphism made it possible to map a total of 238 within-centromere markers using maize recombinant inbred lines. Over half of the markers were shown to interact directly with kinetochores (CENH3) by chromatin immunoprecipitation. Although classical crossing over is fully suppressed across CENH3 domains, two gene conversion events (i.e., non-crossover marker exchanges) were identified in a mapping population. A population genetic analysis of 53 diverse inbreds suggests that historical gene conversion is widespread in maize centromeres, occurring at a rate >1×10−5/marker/generation. We conclude that gene conversion accelerates centromere evolution by facilitating sequence exchange among chromosomes. [plos biology commentary]

Indel-associated mutation rate varies with mating system in flowering plants
Hollister JD, Ross-Ibarra J, Gaut BS

We show that mating system differences in heterozygosity mitigate the effects of insertion and deletion polymorphisms on nucleotide diversity.

Genetic diversity in a crop metapopulation
van Heerwaarden J, van Eeuwijk FA, Ross-Ibarra J

The need to protect crop genetic resources has sparked a growing interest in the genetic diversity maintained in traditional farming systems worldwide. Although traditional seed management has been proposed as an important determinant of genetic diversity and structure in crops, no models exist that can adequately describe the genetic effects of seed management. We present a metapopulation model that accounts for several features unique to managed crop populations. Using traditional maize agriculture as an example, we develop a coalescence-based model of a crop metapopulation undergoing pollen and seed flow as well as seed replacement. In contrast to metapopulation work on natural systems, we model seed migration as episodic and originating from a single source per population rather than as a constant immigration from the entire metapopulation. We find that the correlated origin of migrants leads to surprising results, including a loss of invariance of within-deme diversity and a parabolic relationship between F(ST) and migration quantity. In contrast, the effects of migration frequency on diversity and structure are more similar to classical predictions, suggesting that seed migration in managed crop populations cannot be described by a single parameter. In addition to migration, we investigate the effects of deme size and extinction rates on genetic structure, and show that high levels of pollen migration may mask the effects of seed management on structure. Our results highlight the importance of analytically evaluating the effects of deviations from classical metapopulation models, especially in systems for which data are available to estimate specific model parameters.

Other papers by lab members

Matthew Hufford

Epanchin-Niell, Rebecca S., et al. "Controlling invasive species in complex social landscapes." Frontiers in Ecology and the Environment 8.4 (2010): 210-216.

2009

A first-generation haplotype map of maize
Gore MA, Chia JM, Elshire RJ, Sun Q …[4 authors]… Grills GS, Ross-Ibarra J, Ware DH, Buckler ES

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Maize is an important crop species of high genetic diversity. We identified and genotyped several million sequence polymorphisms among 27 diverse maize inbred lines and discovered that the genome was characterized by highly divergent haplotypes and showed 10- to 30-fold variation in recombination rates. Most chromosomes have pericentromeric regions with highly suppressed recombination that appear to have influenced the effectiveness of selection during maize inbred development and may be a major component of heterosis. We found hundreds of selective sweeps and highly differentiated regions that probably contain loci that are key to geographic adaptation. This survey of genetic diversity provides a foundation for uniting breeding efforts across the world and for dissecting complex traits through genome-wide association studies.

A pleistocene clone of Palmer’s Oak persisting in Southern California
May MR, Provance MC, Sanders AC, Ellstrand NC, Ross-Ibarra J

We discover a 13,000 year old oak clone in the hills of Southern California

Selection on grain shattering genes and rates of rice domestication
Zhang LB, Zhu Q, Wu ZQ, Ross-Ibarra J, Gaut BS, Ge S, Sang T

Molecular cloning of major quantitative trait loci (QTLs) responsible for the reduc-tion of rice grain shattering, a hallmark of cereal domestication, provided opportunitiesfor in-depth investigation of domestication processes.• Here, we studied nucleotide variation at the shattering loci, sh4 and qSH1, forcultivated rice, Oryza sativa ssp. indica and Oryza sativa ssp. japonica, and the wildprogenitors, Oryza nivara andOryza rufipogon.• The nonshattering sh4 allele was fixed in all rice cultivars, with levels of sequencepolymorphism significantly reduced in both indica and japonica cultivars relative tothe wild progenitors. The sh4 phylogeny together with the neutrality tests and coales-cent simulations suggested that sh4 had a single origin and was fixed by artificialselection during the domestication of rice. Selection on qSH1 was not detected inindica and remained unclear in japonica.• Selection on sh4 could be strong enough to have driven its fixation in a populationof cultivated rice within a period of c. 100 yr. The slow fixation of the nonshatteringphenotype observed at the archeological sites might be a result of relatively weakselection on mutations other than sh4 in early rice cultivation. The fixation of sh4could have been achieved later through strong selection for the optimal phenotype

Historical divergence and gene flow in the genus Zea
Ross-Ibarra J, Tenaillon M, Gaut BS

Gene flow plays a fundamental role in plant evolutionary history, yet its role in population divergence—and ultimately speciation—remains poorly understood. We investigated gene flow and the modalities of divergence in the domesticate Zea mays ssp. mays and three wild Zea taxa using sequence polymorphism data from 26 nuclear loci. We described diversity across loci and assessed evidence for adaptive and purifying selection at nonsynonymous sites. For each of three divergence events in the history of these taxa, we used approximate Bayesian simulation to estimate population sizes and divergence times and explicitly compare among alternative models of divergence. Our estimates of divergence times are surprisingly consistent with previous data from other markers and suggest rapid diversification of lineages within Zea in the last ∼150,000 years. We found widespread evidence of historical gene flow, including evidence for divergence in the face of gene flow. We speculate that cultivated maize may serve as a bridge for gene flow among otherwise allopatric wild taxa.

2008

Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata
Ross-Ibarra J, Wright SI, Foxe JP, Kawabe A, DeRose-Wilson L, Gos G, Charlesworth D, Gaut BS

Background

Many of the processes affecting genetic diversity act on local populations. However, studies of plant nucleotide diversity have largely ignored local sampling, making it difficult to infer the demographic history of populations and to assess the importance of local adaptation. Arabidopsis lyrata, a self-incompatible, perennial species with a circumpolar distribution, is an excellent model system in which to study the roles of demographic history and local adaptation in patterning genetic variation.

Principal Findings

We studied nucleotide diversity in six natural populations of Arabidopsis lyrata, using 77 loci sampled from 140 chromosomes. The six populations were highly differentiated, with a median FST of 0.52, and structure analysis revealed no evidence of admixed individuals. Average within-population diversity varied among populations, with the highest diversity found in a German population; this population harbors 3-fold higher levels of silent diversity than worldwide samples of A. thaliana. All A. lyrata populations also yielded positive values of Tajima’s D. We estimated a demographic model for these populations, finding evidence of population divergence over the past 19,000 to 47,000 years involving non-equilibrium demographic events that reduced the effective size of most populations. Finally, we used the inferred demographic model to perform an initial test for local adaptation and identified several genes, including the flowering time gene FCA and a disease resistance locus, as candidates for local adaptation events.

Conclusions

Our results underscore the importance of population-specific, non-equilibrium demographic processes in patterning diversity within A. lyrata. Moreover, our extensive dataset provides an important resource for future molecular population genetic studies of local adaptation in A. lyrata.

Demography and weak selection drive patterns of TE diversity in natural populations of A. lyrata
Lockton S, Ross-Ibarra J, Gaut BS

We show that differences in demographic history among populations of have changed the abundance and freqeuncy of transposable elements in the A lyrata genome.

Multiple domestications do not appear monophyletic
Ross-Ibarra J, Gaut BS

A rebuttal showing that genetic data can indeed successfully recover multiple independent domestications.

Selection on major components of angiosperm genomes
Gaut BS, Ross-Ibarra J

Discusses some of the evolutionary forces responsible for shaping genome size across plants.

2007

Plant domestication, a unique opportunity to identify the genetic basis of adaptation
Ross-Ibarra J, Morrell PL, Gaut BS

Presents plant domestication as an ideal system in which to study the genetics of adaptation.

Genome size and recombination in angiosperms: a second look
Ross-Ibarra J

Despite dramatic differences in genome size – and thus space for recombination to occur – previous workers found no correlation between recombination rate and genome size in flowering plants. Here I re-investigate these claims using phylogenetic comparative methods to test a large data set of recombination data in angiosperms. I show that genome size is significantly correlated with recombination rate across a wide sampling of species and that change in genome size explains a meaningful proportion (∼20%) of variation in recombination rate. I show that the strength of this correlation is comparable with that of several characters previously linked to evolutionary change in recombination rate, but argue that consideration of processes of genome size change likely make the observed correlation a conservative estimate. And finally, although I find that recombination rate increases less than proportionally to change in genome size, several mechanistic and theoretical arguments suggest that this result is not unexpected.

2001-2006

Mitochondrial DNA and population size
Wares JP, Barber PH, Ross-Ibarra J, Sotka EE, Toonen RJ

Quantitative trait loci and the study of plant domestication
Ross-Ibarra J

Plant domestication ranks as one of the most important developments in human history, giving human populations the potential to harness unprecedented quantities of the earth’s resources. But domestication has also played a more subtle historical role as the foundation of the modern study of evolution and adaptation. Until recently, however, researchers interested in domestication were limited to studying phenotypic changes or the genetics of simple Mendelian traits, when often the characters of most interest – fruit size, yield, height, flowering time, etc. – are quantitative in nature. The goals of this paper are to review some of the recent work on the quantitative genetics of plant domestication, identify some of the common trends found in this literature, and offer some novel interpretations of the data that is currently available.

The evolution of recombination under domestication: a test of two hypotheses [data]
Ross-Ibarra J

Here I test two different hypotheses about the how recombination should relate to domestication: Does domestication itself select for increased recombination (yes), or respecies with higher recombination rates more likely to be domesticated (no).

Origen y domesticación de la chaya (Cnidoscolus aconitifolius Mill IM Johnst): La espinaca Maya
Ross-Ibarra J

I use genetic data to study the origin of a leafy shrub domesticated by the Maya

The ethnobotany of Chaya (Cnidoscolus aconitifolius ssp. aconitifolius Breckon): A nutritious Maya vegetable
Ross-Ibarra J, Molina-Cruz A

Chaya (Cnidoscolusaconitifolius ssp. aconitifolius Breckon) is a domesticatedleafy green vegetable of the Maya region of Guatemala,Belize, southeast Mexico and the YucatdnPeninsula, and parts of Honduras. Thoughrelativelyunknownoutsideof thisarea, evidencesuggeststhatchayawas of significant importanceto ancientpeoples of the Yucata’nPeninsulaandperhapselsewherewithintheMaya region.Herewe reviewwhatlittleresearchhas beendoneon thisimpressiveplant,as wellas recountour own ethnobotanicalinvestigationinto its use as a food plant and medicine,and discuss its botany,nomenclature,and agriculturaluse. Due to its ease of cultivation,potential productivity,and above all its substantialnutritionalvalue, we propose chaya as a potential cropfor areas outsideMesoamerica.

Implications of mating patterns for conservation of the endangered plant Eriogonum ovalifolium var. vineum
Neel MC, Ross-Ibarra J, Ellstrand NC

Mating patterns have direct application to conservation because of their influence on structuring genetic diversity within and among populations and on maintaining that diversity over time. We measured population and family outcrossing rates, biparental inbreeding, correlation of outcrossed paternity, and inbreeding coefficients in six populations from throughout the ecological range of the endangered plant Eriogonum ovalifolium var. vineum using naturally pollinated families. The taxon was primarily outcrossed: population outcrossing rates averaged 0.80 (SE 0.03) and family outcrossing rates averaged 0.88 (SE 0.03); neither rate varied among populations. Five population rates were significantly different from 1 while family rates differed from 1 in only one population. We found high correlated outcrossed paternity and evidence for biparental inbreeding in five populations each. As expected from the predominantly outcrossed mating system, levels of diversity were high and inbreeding coefficients among maternal individuals were low (averaging -0.05, SE 0.12). Differences between inbreeding coefficients of progeny (average 0.21, SE 0.06) and mothers indicated selection against homozygous offspring. These results indicate that it is important to maintain large populations to prevent increases in inbreeding and to maintain pollinator communities to facilitate outcrossing.