Publications by authors named "Jeffrey Ross-Ibarra"

86 Publications

Conserved noncoding sequences provide insights into regulatory sequence and loss of gene expression in maize.

Genome Res 2021 May 27. Epub 2021 May 27.

Institute for Genomic Diversity, Cornell University, Ithaca, New York 14853, USA.

Thousands of species will be sequenced in the next few years; however, understanding how their genomes work, without an unlimited budget, requires both molecular and novel evolutionary approaches. We developed a sensitive sequence alignment pipeline to identify conserved noncoding sequences (CNSs) in the Andropogoneae tribe (multiple crop species descended from a common ancestor ∼18 million years ago). The Andropogoneae share similar physiology while being tremendously genomically diverse, harboring a broad range of ploidy levels, structural variation, and transposons. These contribute to the potential of Andropogoneae as a powerful system for studying CNSs and are factors we leverage to understand the function of maize CNSs. We found that 86% of CNSs were comprised of annotated features, including introns, UTRs, putative -regulatory elements, chromatin loop anchors, noncoding RNA (ncRNA) genes, and several transposable element superfamilies. CNSs were enriched in active regions of DNA replication in the early S phase of the mitotic cell cycle and showed different DNA methylation ratios compared to the genome-wide background. More than half of putative -regulatory sequences (identified via other methods) overlapped with CNSs detected in this study. Variants in CNSs were associated with gene expression levels, and CNS absence contributed to loss of gene expression. Furthermore, the evolution of CNSs was associated with the functional diversification of duplicated genes in the context of maize subgenomes. Our results provide a quantitative understanding of the molecular processes governing the evolution of CNSs in maize.
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http://dx.doi.org/10.1101/gr.266528.120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8256870PMC
May 2021

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces.

Mol Biol Evol 2021 Apr 27. Epub 2021 Apr 27.

Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, 50014, USA.

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 substantial evidence of parallel adaptation at the level of individual SNPs, genes and pathways in four independent highland maize populations. The majority of convergently selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands, while standing variation introduced by ancient gene flow was also a contributor. 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. Keyword: convergent adaptation, flowering time, polygenic adaptation, population branch statistic.
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http://dx.doi.org/10.1093/molbev/msab119DOI Listing
April 2021

Gene body methylation is under selection in Arabidopsis thaliana.

Genetics 2021 Jun;218(2)

Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA 92697-2525, USA.

In plants, mammals and insects, some genes are methylated in the CG dinucleotide context, a phenomenon called gene body methylation (gbM). It has been controversial whether this phenomenon has any functional role. Here, we took advantage of the availability of 876 leaf methylomes in Arabidopsis thaliana to characterize the population frequency of methylation at the gene level and to estimate the site-frequency spectrum of allelic states. Using a population genetics model specifically designed for epigenetic data, we found that genes with ancestral gbM are under significant selection to remain methylated. Conversely, ancestrally unmethylated genes were under selection to remain unmethylated. Repeating the analyses at the level of individual cytosines confirmed these results. Estimated selection coefficients were small, on the order of 4 Nes = 1.4, which is similar to the magnitude of selection acting on codon usage. We also estimated that A. thaliana is losing gbM threefold more rapidly than gaining it, which could be due to a recent reduction in the efficacy of selection after a switch to selfing. Finally, we investigated the potential function of gbM through its link with gene expression. Across genes with polymorphic methylation states, the expression of gene body methylated alleles was consistently and significantly higher than unmethylated alleles. Although it is difficult to disentangle genetic from epigenetic effects, our work suggests that gbM has a small but measurable effect on fitness, perhaps due to its association to a phenotype-like gene expression.
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http://dx.doi.org/10.1093/genetics/iyab061DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8225343PMC
June 2021

Comparative evolutionary genetics of deleterious load in sorghum and maize.

Nat Plants 2021 01 15;7(1):17-24. Epub 2021 Jan 15.

Plant Breeding and Genetics, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA.

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 analysed ~13 million variants identified from whole-genome resequencing of 499 sorghum lines together with 25 million 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 with wild lines. Additionally, sorghum and maize population genetic summary statistics were used to predict a gene deleterious index with an accuracy greater 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 these variants for removal through genome editing and breeding.
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http://dx.doi.org/10.1038/s41477-020-00834-5DOI Listing
January 2021

Evolutionary and functional genomics of DNA methylation in maize domestication and improvement.

Nat Commun 2020 11 2;11(1):5539. Epub 2020 Nov 2.

Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA.

DNA methylation is a ubiquitous chromatin feature, present in 25% of cytosines in the maize genome, but variation and evolution of the methylation landscape during maize domestication remain largely unknown. Here, we leverage whole-genome sequencing (WGS) and whole-genome bisulfite sequencing (WGBS) data on populations of modern maize, landrace, and teosinte (Zea mays ssp. parviglumis) to estimate epimutation rates and selection coefficients. We find weak evidence for direct selection on DNA methylation in any context, but thousands of differentially methylated regions (DMRs) are identified population-wide that are correlated with recent selection. For two trait-associated DMRs, vgt1-DMR and tb1-DMR, HiChIP data indicate that the interactive loops between DMRs and respective downstream genes are present in B73, a modern maize line, but absent in teosinte. 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.
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http://dx.doi.org/10.1038/s41467-020-19333-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7606521PMC
November 2020

Selective Loss of Diversity in Doubled-Haploid Lines from European Maize Landraces.

G3 (Bethesda) 2020 07 7;10(7):2497-2506. Epub 2020 Jul 7.

Department of Plant Sciences, University of California, Davis, CA,

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 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 losses of shared haplotypes. We find evidence consistent with selection at functional sites that are potentially involved in the diversity differences between landrace and DH populations. Although we were unable to uncover more details about the mode of selection, we conclude that landrace DH lines may be a valuable tool for the introduction of variation into maize breeding programs but come at the cost of decreased genetic diversity.
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http://dx.doi.org/10.1534/g3.120.401196DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7341142PMC
July 2020

The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication.

PLoS Genet 2020 05 14;16(5):e1008791. Epub 2020 May 14.

Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

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 FST) 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.
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http://dx.doi.org/10.1371/journal.pgen.1008791DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7266358PMC
May 2020

Genome-wide selection and genetic improvement during modern maize breeding.

Nat Genet 2020 06 27;52(6):565-571. Epub 2020 Apr 27.

College of Life Sciences, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, China.

Since the development of single-hybrid maize breeding programs in the first half of the twentieth century, maize yields have increased over sevenfold, and much of that increase can be attributed to tolerance of increased planting density. To explore the genomic basis underlying the dramatic yield increase in maize, we conducted a comprehensive analysis of the genomic and phenotypic changes associated with modern maize breeding through chronological sampling of 350 elite inbred lines representing multiple eras of germplasm from both China and the United States. We document several 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. This work demonstrates the use of the breeding-era approach for identifying breeding signatures and lays the foundation for future genomics-enabled maize breeding.
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http://dx.doi.org/10.1038/s41588-020-0616-3DOI Listing
June 2020

Evolutionary insights into plant breeding.

Curr Opin Plant Biol 2020 04 20;54:93-100. Epub 2020 Apr 20.

Bond Life Science Center and Division of Biological Sciences, University of Missouri, Columbia, MO, USA.

Crop domestication is a fascinating area of study, as shown by 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 related to 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.
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http://dx.doi.org/10.1016/j.pbi.2020.03.003DOI Listing
April 2020

The Temporal Dynamics of Background Selection in Nonequilibrium Populations.

Genetics 2020 04 18;214(4):1019-1030. Epub 2020 Feb 18.

Department of Evolution and Ecology, University of California, Davis, California 95616

Neutral genetic diversity across the genome is determined by the complex interplay of mutation, demographic history, and natural selection. While the direct action of natural selection is limited to functional loci across the genome, its impact can have effects on nearby neutral loci due to genetic linkage. These effects of selection at linked sites, referred to as genetic hitchhiking and background selection (BGS), are pervasive across natural populations. However, only recently has there been a focus on the joint consequences of demography and selection at linked sites, and some empirical studies have come to apparently contradictory conclusions as to their combined effects. To understand the relationship between demography and selection at linked sites, we conducted an extensive forward simulation study of BGS under a range of demographic models. We found that the relative levels of diversity in BGS and neutral regions vary over time and that the initial dynamics after a population size change are often in the opposite direction of the long-term expected trajectory. Our detailed observations of the temporal dynamics of neutral diversity in the context of selection at linked sites in nonequilibrium populations provide new intuition about why patterns of diversity under BGS vary through time in natural populations and help reconcile previously contradictory observations. Most notably, our results highlight that classical models of BGS are poorly suited for predicting diversity in nonequilibrium populations.
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http://dx.doi.org/10.1534/genetics.119.302892DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153942PMC
April 2020

Genomics of Long- and Short-Term Adaptation in Maize and Teosintes.

Methods Mol Biol 2020 ;2090:289-311

Génétique Quantitative et Evolution-Le Moulon, Institut National de la Recherche Agronomique, Université Paris-Sud, Centre National de la Recherche Scientifique, AgroParisTech, Université Paris-Saclay, Gif-sur-Yvette, France.

Maize is an excellent model for the study of plant adaptation. Indeed, post domestication maize quickly adapted to a host of new environments across the globe. And work over the last decade has begun to highlight the role of the wild relatives of maize-the teosintes Zea mays ssp. parviglumis and ssp. mexicana-as excellent models for dissecting long-term local adaptation.Although human-driven selection associated with maize domestication has been extensively studied, the genetic basis of natural variation is still poorly understood. Here we review studies on the genetic basis of adaptation and plasticity in maize and its wild relatives. We highlight a range of different processes that contribute to adaptation and discuss evidence from natural, cultivated, and experimental populations. From an applied perspective, understanding the genetic bases of adaptation and the contribution of plasticity will provide us with new tools to both better understand and mitigate the effect of climate changes on natural and cultivated populations.
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http://dx.doi.org/10.1007/978-1-0716-0199-0_12DOI Listing
January 2021

Dynamic Patterns of Transcript Abundance of Transposable Element Families in Maize.

G3 (Bethesda) 2019 11 5;9(11):3673-3682. Epub 2019 Nov 5.

Department of Plant and Microbial Biology and

Transposable Elements (TEs) are mobile elements that contribute the majority of DNA sequences in the maize genome. Due to their repetitive nature, genomic studies of TEs are complicated by the difficulty of properly attributing multi-mapped short reads to specific genomic loci. Here, we utilize a method to attribute RNA-seq reads to TE families rather than particular loci in order to characterize transcript abundance for TE families in the maize genome. We applied this method to assess per-family expression of transposable elements in >800 published RNA-seq libraries representing a range of maize development, genotypes, and hybrids. While a relatively small proportion of TE families are transcribed, expression is highly dynamic with most families exhibiting tissue-specific expression. A large number of TE families were specifically detected in pollen and endosperm, consistent with reproductive dynamics that maintain silencing of TEs in the germ line. We find that B73 transcript abundance is a poor predictor of TE expression in other genotypes and that transcript levels can differ even for shared TEs. Finally, by assessing recombinant inbred line and hybrid transcriptomes, complex patterns of TE transcript abundance across genotypes emerged. Taken together, this study reveals a dynamic contribution of TEs to maize transcriptomes.
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http://dx.doi.org/10.1534/g3.119.400431DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829137PMC
November 2019

Adaptive phenotypic divergence in an annual grass differs across biotic contexts.

Evolution 2019 11 26;73(11):2230-2246. Epub 2019 Aug 26.

Center for Population Biology, University of California, Davis, California, 95616.

Climate is a powerful force shaping adaptation within species, yet adaptation to climate occurs against a biotic background: species interactions can filter fitness consequences of genetic variation by altering phenotypic expression of genotypes. We investigated this process using populations of teosinte, a wild annual grass related to maize (Zea mays ssp. mexicana), sampling plants from 10 sites along an elevational gradient as well as rhizosphere biota from three of those sites. We grew half-sibling teosinte families in each biota to test whether trait divergence among teosinte populations reflects adaptation or drift, and whether rhizosphere biota affect expression of diverged traits. We further assayed the influence of rhizosphere biota on contemporary additive genetic variation. We found that adaptation across environment shaped divergence of some traits, particularly flowering time and root biomass. We also observed that different rhizosphere biota shifted expressed values of these traits within teosinte populations and families and altered within-population genetic variance and covariance. In sum, our results imply that changes in trait expression and covariance elicited by rhizosphere communities could have played a historical role in teosinte adaptation to environments and that they are likely to play a role in the response to future selection.
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http://dx.doi.org/10.1111/evo.13818DOI Listing
November 2019

Transposable elements contribute to dynamic genome content in maize.

Plant J 2019 12 18;100(5):1052-1065. Epub 2019 Sep 18.

Department of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, 55108, USA.

Transposable elements (TEs) are ubiquitous components of eukaryotic genomes and can create variation in genome organization and content. Most maize genomes are composed of TEs. We developed an approach to define shared and variable TE insertions across genome assemblies and applied this method to four maize genomes (B73, W22, Mo17 and PH207) with uniform structural annotations of TEs. Among these genomes we identified approximately 400 000 TEs that are polymorphic, encompassing 1.6 Gb of variable TE sequence. These polymorphic TEs include a combination of recent transposition events as well as deletions of older TEs. There are examples of polymorphic TEs within each of the superfamilies of TEs and they are found distributed across the genome, including in regions of recent shared ancestry among individuals. There are many examples of polymorphic TEs within or near maize genes. In addition, there are 2380 gene annotations in the B73 genome that are located within variable TEs, providing evidence for the role of TEs in contributing to the substantial differences in annotated gene content among these genotypes. TEs are highly variable in our survey of four temperate maize genomes, highlighting the major contribution of TEs in driving variation in genome organization and gene content. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://github.com/SNAnderson/maizeTE_variation; https://mcstitzer.github.io/maize_TEs.
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http://dx.doi.org/10.1111/tpj.14489DOI Listing
December 2019

Hybrid Decay: A Transgenerational Epigenetic Decline in Vigor and Viability Triggered in Backcross Populations of Teosinte with Maize.

Genetics 2019 09 18;213(1):143-160. Epub 2019 Jul 18.

Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706

In the course of generating populations of maize with teosinte chromosomal introgressions, an unusual sickly plant phenotype was noted in individuals from crosses with two teosinte accessions collected near Valle de Bravo, Mexico. The plants of these Bravo teosinte accessions appear phenotypically normal themselves and the F plants appear similar to typical maize × teosinte Fs. However, upon backcrossing to maize, the BC and subsequent generations display a number of detrimental characteristics including shorter stature, reduced seed set, and abnormal floral structures. This phenomenon is observed in all BC individuals and there is no chromosomal segment linked to the sickly plant phenotype in advanced backcross generations. Once the sickly phenotype appears in a lineage, normal plants are never again recovered by continued backcrossing to the normal maize parent. Whole-genome shotgun sequencing reveals a small number of genomic sequences, some with homology to transposable elements, that have increased in copy number in the backcross populations. Transcriptome analysis of seedlings, which do not have striking phenotypic abnormalities, identified segments of 18 maize genes that exhibit increased expression in sickly plants. A assembly of transcripts present in plants exhibiting the sickly phenotype identified a set of 59 upregulated novel transcripts. These transcripts include some examples with sequence similarity to transposable elements and other sequences present in the recurrent maize parent (W22) genome as well as novel sequences not present in the W22 genome. Genome-wide profiles of gene expression, DNA methylation, and small RNAs are similar between sickly plants and normal controls, although a few upregulated transcripts and transposable elements are associated with altered small RNA or methylation profiles. This study documents hybrid incompatibility and genome instability triggered by the backcrossing of Bravo teosinte with maize. We name this phenomenon "hybrid decay" and present ideas on the mechanism that may underlie it.
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http://dx.doi.org/10.1534/genetics.119.302378DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727801PMC
September 2019

Characterization of introgression from the teosinte ssp. to Mexican highland maize.

PeerJ 2019 3;7:e6815. Epub 2019 May 3.

Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Guanajuato, Mexico.

Background: The spread of maize cultivation to the highlands of central Mexico was accompanied by substantial introgression from the endemic wild teosinte ssp. , prompting the hypothesis that the transfer of beneficial variation facilitated local adaptation.

Methods: We used whole-genome sequence data to map regions of ssp. introgression in three Mexican highland maize individuals. We generated a genetic linkage map and performed Quantitative Trait Locus mapping in an F population derived from a cross between lowland and highland maize individuals.

Results: Introgression regions ranged in size from several hundred base pairs to Megabase-scale events. Gene density within introgression regions was comparable to the genome as a whole, and over 1,000 annotated genes were located within introgression events. Quantitative Trait Locus mapping identified a small number of loci linked to traits characteristic of Mexican highland maize.

Discussion: Although there was no strong evidence to associate quantitative trait loci with regions of introgression, we nonetheless identified many Mexican highland alleles of introgressed origin that carry potentially functional sequence variants. The impact of introgression on stress tolerance and yield in the highland environment remains to be fully characterized.
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http://dx.doi.org/10.7717/peerj.6815DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6501764PMC
May 2019

Detecting Adaptive Differentiation in Structured Populations with Genomic Data and Common Gardens.

Genetics 2019 03 24;211(3):989-1004. Epub 2019 Jan 24.

Department of Evolution and Ecology, University of California, Davis, California 95616.

Adaptation in quantitative traits often occurs through subtle shifts in allele frequencies at many loci-a process called polygenic adaptation. While a number of methods have been developed to detect polygenic adaptation in human populations, we lack clear strategies for doing so in many other systems. In particular, there is an opportunity to develop new methods that leverage datasets with genomic data and common garden trait measurements to systematically detect the quantitative traits important for adaptation. Here, we develop methods that do just this, using principal components of the relatedness matrix to detect excess divergence consistent with polygenic adaptation, and using a conditional test to control for confounding effects due to population structure. We apply these methods to inbred maize lines from the United States Department of Agriculture germplasm pool and maize landraces from Europe. Ultimately, these methods can be applied to additional domesticated and wild species to give us a broader picture of the specific traits that contribute to adaptation and the overall importance of polygenic adaptation in shaping quantitative trait variation.
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http://dx.doi.org/10.1534/genetics.118.301786DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6404252PMC
March 2019

Genetic architecture and selective sweeps after polygenic adaptation to distant trait optima.

PLoS Genet 2018 11 19;14(11):e1007794. Epub 2018 Nov 19.

Dept. of Plant Sciences and Center for Population Biology, University of California, Davis, Davis, CA, USA.

Understanding the genetic basis of phenotypic adaptation to changing environments is an essential goal of population and quantitative genetics. While technological advances now allow interrogation of genome-wide genotyping data in large panels, our understanding of the process of polygenic adaptation is still limited. To address this limitation, we use extensive forward-time simulation to explore the impacts of variation in demography, trait genetics, and selection on the rate and mode of adaptation and the resulting genetic architecture. We simulate a population adapting to an optimum shift, modeling sequence variation for 20 QTL for each of 12 different demographies for 100 different traits varying in the effect size distribution of new mutations, the strength of stabilizing selection, and the contribution of the genomic background. We then use random forest regression approaches to learn the relative importance of input parameters in determining a number of aspects of the process of adaptation, including the speed of adaptation, the relative frequency of hard sweeps and sweeps from standing variation, or the final genetic architecture of the trait. We find that selective sweeps occur even for traits under relatively weak selection and where the genetic background explains most of the variation. Though most sweeps occur from variation segregating in the ancestral population, new mutations can be important for traits under strong stabilizing selection that undergo a large optimum shift. We also show that population bottlenecks and expansion impact overall genetic variation as well as the relative importance of sweeps from standing variation and the speed with which adaptation can occur. We then compare our results to two traits under selection during maize domestication, showing that our simulations qualitatively recapitulate differences between them. Overall, our results underscore the complex population genetics of individual loci in even relatively simple quantitative trait models, but provide a glimpse into the factors that drive this complexity and the potential of these approaches for understanding polygenic adaptation.
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http://dx.doi.org/10.1371/journal.pgen.1007794DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6277123PMC
November 2018

Evolutionary Responses to Conditionality in Species Interactions across Environmental Gradients.

Am Nat 2018 12 31;192(6):715-730. Epub 2018 Oct 31.

The outcomes of many species interactions are conditional on the environments in which they occur. Often, interactions grade from being more positive under stressful or low-resource conditions to more antagonistic or neutral under benign conditions. Here, we take predictions about two well-supported ecological theories on conditionality-limiting resource models and the stress-gradient hypothesis-and combine them with those from the geographic mosaic theory of coevolution (GMTC) to generate predictions for systematic patterns of adaptation and coadaptation between partners along abiotic gradients. When interactions become more positive in stressful environments, mutations that increase fitness in one partner may also increase fitness in the other; because fitnesses are aligned, selection should favor greater mutualistic adaptation and coadaptation between interacting species in stressful ends of environmental gradients. As a corollary, in benign environments antagonistic coadaptation could result in Red Queen or arms-race dynamics or the reduction of antagonism through character displacement and niche partitioning. Here, we distinguish between generally mutualistic or antagonistic adaptation (i.e., mutations in one partner that have similar effects across multiple populations of the other) and specific adaptations to sympatric partners (local adaptation), which can occur either alone or simultaneously. We then outline the kinds of data required to test these predictions, develop experimental designs and statistical methods, and demonstrate these using simulations based on GMTC models. Our methods can be applied to a range of conditional outcomes and may also be useful in assisted translocation approaches in the face of climate change.
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http://dx.doi.org/10.1086/700118DOI Listing
December 2018

Maize domestication and gene interaction.

New Phytol 2018 10 23;220(2):395-408. Epub 2018 Jul 23.

Department of Plant Sciences, University of California, Davis, Davis, CA, 95616, USA.

Contents Summary 395 I. Introduction 395 II. The genetic basis of maize domestication 396 III. The tempo of maize domestication 401 IV. Genetic interactions and selection during maize domestication 401 V. Gene networks of maize domestication alleles 404 VI. Implications of gene interactions on evolution and selection404 VII. Conclusions 405 Acknowledgements 405 References 405 SUMMARY: Domestication is a tractable system for following evolutionary change. Under domestication, wild populations respond to shifting selective pressures, resulting in adaptation to the new ecological niche of cultivation. Owing to the important role of domesticated crops in human nutrition and agriculture, the ancestry and selection pressures transforming a wild plant into a domesticate have been extensively studied. In Zea mays, morphological, genetic and genomic studies have elucidated how a wild plant, the teosinte Z. mays subsp. parviglumis, was transformed into the domesticate Z. mays subsp. mays. Five major morphological differences distinguish these two subspecies, and careful genetic dissection has pinpointed the molecular changes responsible for several of these traits. But maize domestication was a consequence of more than just five genes, and regions throughout the genome contribute. The impacts of these additional regions are contingent on genetic background, both the interactions between alleles of a single gene and among alleles of the multiple genes that modulate phenotypes. Key genetic interactions include dominance relationships, epistatic interactions and pleiotropic constraint, including how these variants are connected in gene networks. Here, we review the role of gene interactions in generating the dramatic phenotypic evolution seen in the transition from teosinte to maize.
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http://dx.doi.org/10.1111/nph.15350DOI Listing
October 2018

Parallel altitudinal clines reveal trends in adaptive evolution of genome size in Zea mays.

PLoS Genet 2018 05 10;14(5):e1007162. Epub 2018 May 10.

Department of Plant Sciences, University of California, Davis, Davis, California, United States of America.

While the vast majority of genome size variation in plants is due to differences in repetitive sequence, we know little about how selection acts on repeat content in natural populations. Here we investigate parallel changes in intraspecific genome size and repeat content of domesticated maize (Zea mays) landraces and their wild relative teosinte across altitudinal gradients in Mesoamerica and South America. We combine genotyping, low coverage whole-genome sequence data, and flow cytometry to test for evidence of selection on genome size and individual repeat abundance. We find that population structure alone cannot explain the observed variation, implying that clinal patterns of genome size are maintained by natural selection. Our modeling additionally provides evidence of selection on individual heterochromatic knob repeats, likely due to their large individual contribution to genome size. To better understand the phenotypes driving selection on genome size, we conducted a growth chamber experiment using a population of highland teosinte exhibiting extensive variation in genome size. We find weak support for a positive correlation between genome size and cell size, but stronger support for a negative correlation between genome size and the rate of cell production. Reanalyzing published data of cell counts in maize shoot apical meristems, we then identify a negative correlation between cell production rate and flowering time. Together, our data suggest a model in which variation in genome size is driven by natural selection on flowering time across altitudinal clines, connecting intraspecific variation in repetitive sequence to important differences in adaptive phenotypes.
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http://dx.doi.org/10.1371/journal.pgen.1007162DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5944917PMC
May 2018

A Kinesin-14 Motor Activates Neocentromeres to Promote Meiotic Drive in Maize.

Cell 2018 05 5;173(4):839-850.e18. Epub 2018 Apr 5.

Kentucky Wesleyan College, Owensboro, KY 42301, USA.

Maize abnormal chromosome 10 (Ab10) encodes a classic example of true meiotic drive that converts heterochromatic regions called knobs into motile neocentromeres that are preferentially transmitted to egg cells. Here, we identify a cluster of eight genes on Ab10, called the Kinesin driver (Kindr) complex, that are required for both neocentromere motility and preferential transmission. Two meiotic drive mutants that lack neocentromere activity proved to be kindr epimutants with increased DNA methylation across the entire gene cluster. RNAi of Kindr induced a third epimutant and corresponding loss of meiotic drive. Kinesin gliding assays and immunolocalization revealed that KINDR is a functional minus-end-directed kinesin that localizes specifically to knobs containing 180 bp repeats. Sequence comparisons suggest that Kindr diverged from a Kinesin-14A ancestor ∼12 mya and has driven the accumulation of > 500 Mb of knob repeats and affected the segregation of thousands of genes linked to knobs on all 10 chromosomes.
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http://dx.doi.org/10.1016/j.cell.2018.03.009DOI Listing
May 2018

Adaptation in plant genomes: Bigger is different.

Am J Bot 2018 01 13;105(1):16-19. Epub 2018 Feb 13.

Department of Plant Sciences, University of California, Davis, California, 95616, USA.

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http://dx.doi.org/10.1002/ajb2.1002DOI Listing
January 2018

Construction of the third-generation Zea mays haplotype map.

Gigascience 2018 04;7(4):1-12

Institute of Crop Science, Chinese Academy of Agricultural Sciences/National Key Facilities for Crop Gene Resource and Genetic Improvement, Beijing 100081, China.

Background: Characterization of genetic variations in maize has been challenging, mainly due to deterioration of collinearity between individual genomes in the species. An international consortium of maize research groups combined resources to develop the maize haplotype version 3 (HapMap 3), built from whole-genome sequencing data from 1218 maize lines, covering predomestication and domesticated Zea mays varieties across the world.

Results: A new computational pipeline was set up to process more than 12 trillion bp of sequencing data, and a set of population genetics filters was applied to identify more than 83 million variant sites.

Conclusions: We identified polymorphisms in regions where collinearity is largely preserved in the maize species. However, the fact that the B73 genome used as the reference only represents a fraction of all haplotypes is still an important limiting factor.
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http://dx.doi.org/10.1093/gigascience/gix134DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5890452PMC
April 2018

The interplay of demography and selection during maize domestication and expansion.

Genome Biol 2017 11 13;18(1):215. Epub 2017 Nov 13.

Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, USA.

Background: The history of maize has been characterized by major demographic events, including population size changes associated with domestication and range expansion, and gene flow with wild relatives. The interplay between demographic history and selection has shaped diversity across maize populations and genomes.

Results: We investigate these processes using high-depth resequencing data from 31 maize landraces spanning the pre-Columbian distribution of maize, and four wild teosinte individuals (Zea mays ssp. parviglumis). Genome-wide demographic analyses reveal that maize experienced pronounced declines in effective population size due to both a protracted domestication bottleneck and serial founder effects during post-domestication spread, while parviglumis in the Balsas River Valley experienced population growth. The domestication bottleneck and subsequent spread led to an increase in deleterious alleles in the domesticate compared to the wild progenitor. This cost is particularly pronounced in Andean maize, which has experienced a more dramatic founder event compared to other maize populations. Additionally, we detect introgression from the wild teosinte Zea mays ssp. mexicana into maize in the highlands of Mexico, Guatemala, and the southwestern USA, which reduces the prevalence of deleterious alleles likely due to the higher long-term effective population size of teosinte.

Conclusions: These findings underscore the strong interaction between historical demography and the efficiency of selection and illustrate how domesticated species are particularly useful for understanding these processes. The landscape of deleterious alleles and therefore evolutionary potential is clearly influenced by recent demography, a factor that could bear importantly on many species that have experienced recent demographic shifts.
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http://dx.doi.org/10.1186/s13059-017-1346-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5683586PMC
November 2017

Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize.

PLoS Genet 2017 Sep 27;13(9):e1007019. Epub 2017 Sep 27.

Department of Plant Sciences, University of California, Davis, Davis, California, United States of America.

Deleterious alleles have long been proposed to play an important role in patterning phenotypic variation and are central to commonly held ideas explaining the hybrid vigor observed in the offspring of a cross between two inbred parents. We test these ideas using evolutionary measures of sequence conservation to ask whether incorporating information about putatively deleterious alleles can inform genomic selection (GS) models and improve phenotypic prediction. We measured a number of agronomic traits in both the inbred parents and hybrids of an elite maize partial diallel population and re-sequenced the parents of the population. Inbred elite maize lines vary for more than 350,000 putatively deleterious sites, but show a lower burden of such sites than a comparable set of traditional landraces. Our modeling reveals widespread evidence for incomplete dominance at these loci, and supports theoretical models that more damaging variants are usually more recessive. We identify haplotype blocks using an identity-by-decent (IBD) analysis and perform genomic prediction analyses in which we weigh blocks on the basis of complementation for segregating putatively deleterious variants. Cross-validation results show that incorporating sequence conservation in genomic selection improves prediction accuracy for grain yield and other fitness-related traits as well as heterosis for those traits. Our results provide empirical support for an important role for incomplete dominance of deleterious alleles in explaining heterosis and demonstrate the utility of incorporating functional annotation in phenotypic prediction and plant breeding.
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http://dx.doi.org/10.1371/journal.pgen.1007019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5633198PMC
September 2017

How to make a domesticate.

Curr Biol 2017 Sep;27(17):R896-R900

Department of Plant Sciences, University of California, Davis, CA 95616, USA; Genome Center and Center for Population Biology, University of California, Davis, CA 95616, USA. Electronic address:

The Neolithic Revolution brought about the transition from hunting and gathering to sedentary societies, laying the foundation for the development of modern civilizations. The primary innovation that facilitated these changes was the domestication of plants and animals. In the case of plants, this involved the cultivation and selection of individuals with larger edible parts, easier harvesting, and decreased defenses, traits that allowed for the production of a food surplus and occupational specialization. Plant domestication is a process which started approximately 10,000 years ago and has thereafter been repeated independently in many locales around the world. Here, we offer 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.
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http://dx.doi.org/10.1016/j.cub.2017.06.048DOI Listing
September 2017

The potential role of genetic assimilation during maize domestication.

PLoS One 2017 8;12(9):e0184202. Epub 2017 Sep 8.

Dept. of Plant Sciences, University of California Davis, Davis, CA, United States of America.

Domestication research has largely focused on identification of morphological and genetic differences between extant populations of crops and their wild relatives. Little attention has been paid to the potential effects of environment despite substantial known changes in climate from the time of domestication to modern day. In recent research, the exposure of teosinte (i.e., wild maize) to environments similar to the time of domestication, resulted in a plastic induction of domesticated phenotypes in teosinte. These results suggest that early agriculturalists may have selected for genetic mechanisms that cemented domestication phenotypes initially induced by a plastic response of teosinte to environment, a process known as genetic assimilation. To better understand this phenomenon and the potential role of environment in maize domestication, we examined differential gene expression in maize (Zea mays ssp. mays) and teosinte (Zea mays ssp. parviglumis) between past and present conditions. We identified a gene set of over 2000 loci showing a change in expression across environmental conditions in teosinte and invariance in maize. In fact, overall we observed both greater plasticity in gene expression and more substantial changes in co-expressionnal networks in teosinte across environments when compared to maize. While these results suggest genetic assimilation played at least some role in domestication, genes showing expression patterns consistent with assimilation are not significantly enriched for previously identified domestication candidates, indicating assimilation did not have a genome-wide effect.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0184202PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5590903PMC
October 2017

Allele specific expression analysis identifies regulatory variation associated with stress-related genes in the Mexican highland maize landrace Palomero Toluqueño.

PeerJ 2017 23;5:e3737. Epub 2017 Aug 23.

Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, Mexico.

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 F 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 -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.
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http://dx.doi.org/10.7717/peerj.3737DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5572453PMC
August 2017
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