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Crop wild relatives (CWRs) have the capacity to contribute novel traits to agriculture. Given climate change, these contributions may be especially vital for the persistence of perennial crops, because perennials are often clonally propagated and consequently do not evolve rapidly. By studying the landscape genomics of samples from five Vitis CWRs (V. arizonica, V. mustangensis, V. riparia, V. berlandieri and V. girdiana) in the context of projected climate change, we addressed two goals. The first was to assess the relative potential of different CWR accessions to persist in the face of climate change. By integrating species distribution models with adaptive genetic variation, additional genetic features such as genomic load and a phenotype (resistance to Pierce's Disease), we predicted that accessions from one species (V. mustangensis) are particularly well-suited to persist in future climates. The second goal was to identify which CWR accessions may contribute to bioclimatic adaptation for grapevine (V. vinifera) cultivation. To do so, we evaluated whether CWR accessions have the allelic capacity to persist if moved to locations where grapevines are cultivated in the United States. We identified six candidates from V. mustangensis and hypothesized that they may prove useful for contributing alleles that can mitigate climate impacts on viticulture. By identifying candidate germplasm, this study takes a conceptual step toward assessing the genomic and bioclimatic characteristics of CWRs.

SUMMARYThe domestication history of avocado (Persea americana) remains unclear, in part due to a lack of suitable genomic tools.We created a reference genome from the Gwen varietal, which is closely related to the economically dominant Hass varietal. We also compiled a database of 34 resequenced accessions that represented the three botanical races of P. americana.Our genome assembly had an N50 of 3.37 megabases, a BUSCO score of 91% and was scaffolded with a genetic map, producing 12 pseudo-chromosomes with 49,450 genes. We used the Gwen genome as a reference to investigate the population genomics of avocado. Our analyses were consistent with three separate domestication events; we estimated that the Mexican race diverged from the Lowland (formerly known as ‘West Indian’) and Guatemalan races >1 million years ago. We also identified putative targets of selective sweeps in domestication events; within the Guatemalan race, putative candidate genes were enriched for fruit development and ripening. We also investigated divergence between heterodichogamous flowering types.With the help of a new reference genome, we inferred the domestication history of avocado and identified genes that may contribute to heterodichogamy, including genes with functions in pollination and floral development.

Xylella fastidiosais a bacterium that infects crops like grapevines, coffee, almonds, citrus and olives, causing economically devastating damage. There is, however, little understanding of the genes that contribute to resistance, the genomic architecture of resistance, and the potential role of climate in shaping resistance, in part because major crops like grapevines (V. vinifera) are not resistant to the bacterium. Here we studied a wild grapevine species,Vitis arizonica, that segregates for resistance toX. fastidiosa. Using genome-wide association, we identified candidate genes that mediate the host response toX. fastidiosainfection. We uncovered evidence that resistance requires genes from multiple genomic regions, based on data from breeding populations and from additionalVitisspecies. We also inferred that resistance evolved more than once in the wild, suggesting that wildVitisspecies may be a rich source for resistance alleles and mechanisms. Finally, resistance inV. arizonicawas climate dependent, because individuals from low (< 10°C) temperature locations in the wettest quarter were typically susceptible to infection, likely reflecting a lack of pathogen pressure in these climates. Surprisingly, climate was nearly as effective a predictor of resistance phenotypes as some genetic markers. This work underscores that pathogen pressure is likely to increase with climate, but it also provides genetic insight and tools for breeding and transforming resistant crops.

Background Introgressive hybridization can reassort genetic variants into beneficial combinations, permitting adaptation to new ecological niches. To evaluate evolutionary patterns and dynamics that contribute to introgression, we investigate six wild Vitis species that are native to the Southwestern United States and useful for breeding grapevine (V. vinifera) rootstocks. Results By creating a reference genome assembly from one wild species, V. arizonica, and by resequencing 130 accessions, we focus on identifying putatively introgressed regions (pIRs) between species. We find six species pairs with signals of introgression between them, comprising up to ~ 8% of the extant genome for some pairs. The pIRs tend to be gene poor, located in regions of high recombination and enriched for genes implicated in disease resistance functions. To assess potential pIR function, we explore SNP associations to bioclimatic variables and to bacterial levels after infection with the causative agent of Pierce’s disease (Xylella fastidiosa). pIRs are enriched for SNPs associated with both climate and bacterial levels, suggesting that introgression is driven by adaptation to biotic and abiotic stressors. Conclusions Altogether, this study yields insights into the genomic extent of introgression, potential pressures that shape adaptive introgression, and the evolutionary history of economically important wild relatives of a critical crop.

Climate change is a threat to biodiversity. One way that this threat manifests is through pronounced shifts in the geographical range of species over time. To predict these shifts, researchers have primarily used species distribution models. However, these models are based on assumptions of niche conservatism and do not consider evolutionary processes, potentially limiting their accuracy and value. To incorporate evolution into the prediction of species' responses to climate change, researchers have turned to landscape genomic data and examined information about local genetic adaptation using climate models. Although this is an important advancement, this approach currently does not include other evolutionary processes-such as gene flow, population dispersal and genomic load-that are critical for predicting the fate of species across the landscape. Here, we briefly review the current practices for the use of species distribution models and for incorporating local adaptation. We next discuss the rationale and theory for considering additional processes, reviewing how they can be incorporated into studies of species' responses to climate change. We summarize with a conceptual framework of how manifold layers of information can be combined to predict the potential response of specific populations to climate change. We illustrate all of the topics using an exemplar dataset and provide the source code as potential tutorials. This Perspective is intended to be a step towards a more comprehensive integration of population genomics with climate change science.

Xylella fastidiosa infects several economically important crops in the Americas, and it also recently emerged in Europe. Here, using a set of Xylella genomes reflective of the genus-wide diversity, we performed a pan-genome analysis based on both core and accessory genes, for two purposes: i) to test associations between genetic divergence and plant host species and ii) to identify positively selected genes that are potentially involved in arms-race dynamics. For the former, tests yielded significant evidence for specialization of X. fastidiosa to plant host species. This observation contributes to a growing literature suggesting that the phylogenetic history of X. fastidiosa lineages affects host range. For the latter, our analyses uncovered evidence of positive selection across codons for 5.3% (67 of 1,257) of core genes and 5.4% (201 of 3,691) of accessory genes; these genes are candidates to encode interacting factors with plant and insect hosts. Most of these genes had unknown functions, but we identified some tractable candidates including nagZ_2, which encodes a beta-glucosidase that is important for Neisseria gonorrhoeae biofilm formation; cya, which modulates gene expression in pathogenic bacteria; and barA, a membrane associated histidine kinase that has roles in cell division, metabolism, and pili formation.ABSTRACT IMPORTANCEXylella fastidiosa causes devasting diseases to several critical crops. Because X. fastidiosa colonizes and infects many plant species, it is important to understand whether the genome of X. fastidiosa has genetic determinants that underlie specialization to specific host plants. We analyzed genome sequences of X. fastidiosa to investigate evolutionary relationships and to test for evidence of positive selection on specific genes. We found a significant signal between genome diversity and host plants, consistent with bacterial specialization to specific plant hosts. By screening for positive selection, we identified both core and accessory genes that may affect pathogenicity, including genes involved in biofilm formation.

Apomixis, or asexual seed formation, is prevalent in Citrinae via a mechanism termed nucellar or adventitious embryony. Here, multiple embryos of a maternal genotype form directly from nucellar cells in the ovule and can outcompete the developing zygotic embryo as they utilize the sexually derived endosperm for growth. Whilst nucellar embryony enables the propagation of clonal plants of maternal genetic constitution, it is also a barrier to effective breeding through hybridization. To address the genetics and evolution of apomixis in Citrinae, a chromosome-level genome of the Hongkong kumquat (Fortunella hindsii) was assembled following a genome-wide variation map including structural variants (SVs) based on 234 Citrinae accessions. This map revealed that hybrid citrus cultivars shelter genome-wide deleterious mutations and SVs into heterozygous states free from recessive selection, which may explain the capability of nucellar embryony in most cultivars during Citrinae diversification. Analyses revealed that parallel evolution may explain the repeated origin of apomixis in different genera of Citrinae. Within Fortunella, we found that apomixis of some varieties originated via introgression. In apomictic Fortunella, the locus associated with apomixis contains the FhRWP gene, encoding an RWP-RK domain-containing protein previously shown to be required for nucellar embryogenesis in Citrus. We found the heterozygous SV in the FhRWP and CitRWP promoters from apomictic Citrus and Fortunella, due to either two or three miniature inverted transposon element (MITE) insertions. A transcription factor, FhARID, encoding an AT-rich interaction domain-containing protein binds to the MITEs in the promoter of apomictic varieties, which facilitates induction of nucellar embryogenesis. This study provides evolutionary genomic and molecular insights into apomixis in Citrinae and has potential ramifications for citrus breeding.

Gene body methylation (gbM) is an epigenetic mark where gene exons are methylated in the CG context only, as opposed to CHG and CHH contexts (where H stands for A, C, or T). CG methylation is transmitted transgenerationally in plants, opening the possibility that gbM may be shaped by adaptation. This presupposes, however, that gbM has a function that affects phenotype, which has been a topic of debate in the literature. Here, we review our current knowledge of gbM in plants. We start by presenting the well-elucidated mechanisms of plant gbM establishment and maintenance. We then review more controversial topics: the evolution of gbM and the potential selective pressures that act on it. Finally, we discuss the potential functions of gbM that may affect organismal phenotypes: gene expression stabilization and upregulation, inhibition of aberrant transcription (reverse and internal), prevention of aberrant intron retention, and protection against TE insertions. To bolster the review of these topics, we include novel analyses to assess the effect of gbM on transcripts. Overall, a growing body of literature finds that gbM correlates with levels and patterns of gene expression. It is not clear, however, if this is a causal relationship. Altogether, functional work suggests that the effects of gbM, if any, must be relatively small, but there is nonetheless evidence that it is shaped by natural selection. We conclude by discussing the potential adaptive character of gbM and its implications for an updated view of the mechanisms of adaptation in plants.

Crop wild relatives (CWRs) have the capacity to contribute novel traits to agriculture. Given climate change, these contributions may be especially vital for the persistence of perennial crops, because perennials are often clonally propagated and consequently do not evolve rapidly. By studying the landscape genomics of samples from fiveVitisCWRs (V. arizonica, V. mustangensis, V. riparia, V. berlandieriandV. girdiana) in the context of projected climate change, we addressed two goals. The first was to assess the relative potential of different CWR accessions to persist in the face of climate change. By integrating species distribution models with adaptive genetic variation, additional genetic features such as genomic load and a phenotype (resistance to Pierce’s Disease), we predicted that accessions from one species (V. mustangensis) are particularly well-suited to persist in future climates. The second goal was to identify which CWR accessions may contribute to bioclimatic adaptation for grapevine (V. vinifera) cultivation. To do so, we evaluated whether CWR accessions have the allelic capacity to persist if moved to locations where grapevines (V. vinifera) are cultivated in the United States. We identified six candidates fromV. mustangensisand hypothesized that they may prove useful for contributing alleles that may mitigate climate impacts on viticulture. By identifying candidate germplasm, this work takes a conceptual step toward assessing the genomic and bioclimatic characteristics of CWRs.

The architecture of topologically associating domains (TADs) varies across plant genomes. Understanding the functional consequences of this diversity requires insights into the pattern, structure, and function of TADs. Here, we present a comprehensive investigation of the 3D genome organization of pepper (Capsicum annuum) and its association with gene expression and genomic variants. We report the first chromosome-scale long-read genome assembly of pepper and generate Hi-C contact maps for four tissues. The contact maps indicate that 3D structure varies somewhat across tissues, but generally the genome was segregated into subcompartments that were correlated with transcriptional state. In addition, chromosomes were almost continuously spanned by TADs, with the most prominent found in large genomic regions that were rich in retrotransposons. A substantial fraction of TAD boundaries were demarcated by chromatin loops, suggesting loop extrusion is a major mechanism for TAD formation; many of these loops were bordered by genes, especially in highly repetitive regions, resulting in gene clustering in three dimensional space. Integrated analysis of Hi-C profiles and transcriptomes showed that change in 3D chromatin structures (e.g. subcompartments, TADs, and loops) was not the primary mechanism contributing to differential gene expression between tissues, but chromatin structure does play a role in transcription stability. TAD boundaries were significantly enriched for breaks of synteny and depletion of sequence variation, suggesting that TADs constrain patterns of genome structural evolution in plants. Together, our work provides insights into principles of 3D genome folding in large plant genomes and its association with function and evolution.

The organization of chromatin into self-interacting domains is universal among eukaryotic genomes, though how and why they form varies considerably. Here we report a chromosome-scale reference genome assembly of pepper (Capsicum annuum) and explore its 3D organization through integrating high-resolution Hi-C maps with epigenomic, transcriptomic, and genetic variation data. Chromatin folding domains in pepper are as prominent as TADs in mammals but exhibit unique characteristics. They tend to coincide with heterochromatic regions enriched with retrotransposons and are frequently embedded in loops, which may correlate with transcription factories. Their boundaries are hotspots for chromosome rearrangements but are otherwise depleted for genetic variation. While chromatin conformation broadly affects transcription variance, it does not predict differential gene expression between tissues. Our results suggest that pepper genome organization is explained by a model of heterochromatin-driven folding promoted by transcription factories and that such spatial architecture is under structural and functional constraints.

Structural variants (SVs) are a largely unexplored feature of plant genomes. Little is known about the type and size of SVs, their distribution among individuals and, especially, their population dynamics. Understanding these dynamics is critical for understanding both the contributions of SVs to phenotypes and the likelihood of identifying them as causal genetic variants in genome-wide associations. Here, we identify SVs and study their evolutionary genomics in clonally propagated grapevine cultivars and their outcrossing wild progenitors. To catalogue SVs, we assembled the highly heterozygous Chardonnay genome, for which one in seven genes is hemizygous based on SVs. Using an integrative comparison between Chardonnay and Cabernet Sauvignon genomes by whole-genome, long-read and short-read alignment, we extended SV detection to population samples. We found that strong purifying selection acts against SVs but particularly against inversion and translocation events. SVs nonetheless accrue as recessive heterozygotes in clonally propagated lineages. They also define outlier regions of genomic divergence between wild and cultivated grapevines, suggesting roles in domestication. Outlier regions include the sex-determination region and the berry colour locus, where independent large, complex inversions have driven convergent phenotypic evolution. This study identified structural variants in grapevine populations, including wild progenitors, using a de novo assembly and comparative genomics approach, and examined their evolutionary genomics and roles in domestication and phenotypic evolution.

A subset of genes in plant genomes are labeled with DNA methylation specifically at CG residues. These genes, known as gene-body methylated (gbM), have a number of associated characteristics. They tend to have longer sequences, to be enriched for intermediate expression levels, and to be associated with slower rates of molecular evolution. Most importantly, gbM genes tend to maintain their level of DNA methylation between species, suggesting that this trait is under evolutionary constraint. Given the degree of conservation in gbM, we still know surprisingly little about its function in plant genomes or whether gbM is itself a target of selection. To address these questions, we surveyed DNA methylation across eight grass (Poaceae) species that span a gradient of genome sizes. We first established that genome size correlates with genome-wide DNA methylation levels, but less so for genic levels. We then leveraged genomic data to identify a set of 2,982 putative orthologs among the eight species and examined shifts of methylation status for each ortholog in a phylogenetic context. A total of 55% of orthologs exhibited a shift in gbM, but these shifts occurred predominantly on terminal branches, indicating that shifts in gbM are rarely conveyed over time. Finally, we found that the degree of conservation of gbM across species is associated with increased gene length, reduced rates of molecular evolution, and increased gene expression level, but reduced gene expression variation across species. Overall, these observations suggest a basis for evolutionary pressure to maintain gbM status over evolutionary time.

Methylated CHH (mCHH) islands are peaks of CHH methylation that occur primarily upstream to genes. These regions are actively targeted by the methylation machinery, occur at boundaries between heterochromatin and euchromatin, and tend to be near highly expressed genes. Here we took an evolutionary perspective by studying upstream mCHH islands across a sample of eight grass species. Using a statistical approach to define mCHH islands as regions that differ from genome-wide background CHH methylation levels, we demonstrated that mCHH islands are common and associate with 39% of genes, on average. We hypothesized that islands should be more frequent in genomes of large size, because they have more heterochromatin and hence more need for defined boundaries. We found, however, that smaller genomes tended to have a higher proportion of genes associated with 5′ mCHH islands. Consistent with previous work suggesting that islands reflect the silencing of the edge of transposable elements (TEs), genes with nearby TEs were more likely to have mCHH islands. However, the presence of mCHH islands was not a function solely of TEs, both because the underlying sequences of islands were often not homologous to TEs and because genic properties also predicted the presence of 5′ mCHH islands. These genic properties included length and gene-body methylation (gbM); in fact, in three of eight species, the absence of gbM was a stronger predictor of a 5′ mCHH island than TE proximity. In contrast, gene expression level was a positive but weak predictor of the presence of an island. Finally, we assessed whether mCHH islands were evolutionarily conserved by focusing on a set of 2,720 orthologs across the eight species. They were generally not conserved across evolutionary time. Overall, our data establish additional genic properties that are associated with mCHH islands and suggest that they are not just a consequence of the TE silencing machinery.

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.

Introgressive hybridization can introduce adaptive genetic variation into a species or population. To evaluate the evolutionary forces that contribute to introgression, we studied six Vitis species that are native to the Southwestern United States and potentially useful for breeding grapevine (V. vinifera) rootstocks. By creating a reference genome from one wild species, V. arizonica, and by resequencing 130 accessions, we focused on identifying putatively introgressed regions (pIRs) between species. We found that up to ~8% of extant genome is attributable to introgression between species. The pIRs tended to be gene poor, located in regions of high recombination and enriched for genes implicated in disease resistance functions. To assess potential pIR function, we explored SNP associations to bioclimatic variables and to bacterial levels after infection with the causative agent of Pierce’s Disease. pIRs were enriched for SNPs associated with both climate and bacterial levels, suggesting potential drivers of adaptive events. Altogether, this study yields insights into the genomic extent of introgression, potential pressures that shape adaptive introgression, and the history of economically important wild relatives of a critical crop.

Climate change is a threat to biodiversity. One way that this threat manifests is through pronounced shifts in the geographical range of species over time. To predict these shifts, researchers have primarily used species distribution models. However, these models are based on assumptions of niche conservatism and do not consider evolutionary processes, potentially limiting their accuracy and value. To incorporate evolution into the prediction of species' responses to climate change, researchers have turned to landscape genomic data and examined information about local genetic adaptation using climate models. Although this is an important advancement, this approach currently does not include other evolutionary processes-such as gene flow, population dispersal and genomic load-that are critical for predicting the fate of species across the landscape. Here, we briefly review the current practices for the use of species distribution models and for incorporating local adaptation. We next discuss the rationale and theory for considering additional processes, reviewing how they can be incorporated into studies of species' responses to climate change. We summarize with a conceptual framework of how manifold layers of information can be combined to predict the potential response of specific populations to climate change. We illustrate all of the topics using an exemplar dataset and provide the source code as potential tutorials. This Perspective is intended to be a step towards a more comprehensive integration of population genomics with climate change science.

Structural variants (SVs) are a largely unstudied feature of plant genome evolution, despite the fact that SVs contribute substantially to phenotypes. In this study, we discovered SVs across a population sample of 347 high-coverage, resequenced genomes of Asian rice (Oryza sativa) and its wild ancestor (O. rufipogon). In addition to this short-read data set, we also inferred SVs from whole-genome assemblies and long-read data. Comparisons among data sets revealed different features of genome variability. For example, genome alignment identified a large (∼4.3 Mb) inversion in indica rice varieties relative to japonica varieties, and long-read analyses suggest that ∼9% of genes from the outgroup (O. longistaminata) are hemizygous. We focused, however, on the resequencing sample to investigate the population genomics of SVs. Clustering analyses with SVs recapitulated the rice cultivar groups that were also inferred from SNPs. However, the site-frequency spectrum of each SV type—which included inversions, duplications, deletions, translocations, and mobile element insertions—was skewed toward lower frequency variants than synonymous SNPs, suggesting that SVs may be predominantly deleterious. Among transposable elements, SINE and mariner insertions were found at especially low frequency. We also used SVs to study domestication by contrasting between rice and O. rufipogon. Cultivated genomes contained ∼25% more derived SVs and mobile element insertions than O. rufipogon, indicating that SVs contribute to the cost of domestication in rice. Peaks of SV divergence were enriched for known domestication genes, but we also detected hundreds of genes gained and lost during domestication, some of which were enriched for traits of agronomic interest.

Background Olive tree (Olea europaea L. subsp. europaea, Oleaceae) has been the most emblematic perennial crop for Mediterranean countries since its domestication around 6000 years ago in the Levant. Two taxonomic varieties are currently recognized: cultivated (var. europaea) and wild (var. sylvestris) trees. However, it remains unclear whether olive cultivars derive from a single initial domestication event followed by secondary diversification, or whether cultivated lineages are the result of more than a single, independent primary domestication event. To shed light into the recent evolution and domestication of the olive tree, here we analyze a group of newly sequenced and available genomes using a phylogenomics and population genomics framework. Results We improved the assembly and annotation of the reference genome, newly sequenced the genomes of twelve individuals: ten var. europaea, one var. sylvestris, and one outgroup taxon (subsp. cuspidata)—and assembled a dataset comprising whole genome data from 46 var. europaea and 10 var. sylvestris. Phylogenomic and population structure analyses support a continuous process of olive tree domestication, involving a major domestication event, followed by recurrent independent genetic admixture events with wild populations across the Mediterranean Basin. Cultivated olives exhibit only slightly lower levels of genetic diversity than wild forms, which can be partially explained by the occurrence of a mild population bottleneck 3000–14,000 years ago during the primary domestication period, followed by recurrent introgression from wild populations. Genes associated with stress response and developmental processes were positively selected in cultivars, but we did not find evidence that genes involved in fruit size or oil content were under positive selection. This suggests that complex selective processes other than directional selection of a few genes are in place. Conclusions Altogether, our results suggest that a primary domestication area in the eastern Mediterranean basin was followed by numerous secondary events across most countries of southern Europe and northern Africa, often involving genetic admixture with genetically rich wild populations, particularly from the western Mediterranean Basin.

In plants, mammals and insects, some genes are methylated in the CG dinucleotide context, a phenomenon called gene body methylation. 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 estimated the site-frequency spectrum of allelic states (epialleles). Using a population genetics model specifically designed for epigenetic data, we found that genes with ancestral gene body methylation are under significant selection to remain methylated. Conversely, all genes taken together were inferred to be under selection to be unmethylated. The estimated selection coefficients were small, similar to the magnitude of selection acting on codon usage. We also estimated that A. thaliana is losing gene body methylation three-fold 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 gene body methylation through its link with gene expression level. 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.

Evolutionary rescue occurs when adaptation restores population growth against a lethal stressor. Here, we studied evolutionary rescue by conducting experiments with Escherichia coli at the lethal temperature of 43.0 °C, to determine the adaptive mutations that drive rescue and to investigate their effects on fitness and gene expression. From hundreds of populations, we observed that ∼9% were rescued by genetic adaptations. We sequenced 26 populations and identified 29 distinct mutations. Of these populations, 21 had a mutation in the hslVU or rpoBC operon, suggesting that mutations in either operon could drive rescue. We isolated seven strains of E. coli carrying a putative rescue mutation in either the hslVU or rpoBC operon to investigate the mutations’ effects. The single rescue mutations increased E. coli’s relative fitness by an average of 24% at 42.2 °C, but they decreased fitness by 3% at 37.0 °C, illustrating that antagonistic pleiotropy likely affected the establishment of rescue in our system. Gene expression analysis revealed only 40 genes were upregulated across all seven mutations, and these were enriched for functions in translational and flagellar production. As with previous experiments with high temperature adaptation, the rescue mutations tended to restore gene expression toward the unstressed state, but they also caused a higher proportion of novel gene expression patterns. Overall, we find that rescue is infrequent, that it is facilitated by a limited number of mutational targets, and that rescue mutations may have qualitatively different effects than mutations that arise from evolution to nonlethal stressors.

BackgroundThe olive tree (Olea europaea L. subsp. europaea, Oleaceae) has been the most economic perennial crop for Mediterranean countries since its domestication around 6,000 years ago. Two taxonomic varieties are currently recognized: cultivated (var. europaea) and wild (var. sylvestris) trees. To shed light into the recent evolution and domestication of the olive tree, we sequenced the genomes of twelve individuals: ten var. europaea, one var. sylvestris, and one outgroup taxon (subsp. cuspidata). All of them were analysed together with an improved assembly of var. europaea reference genome and the available assembly of var. sylvestris.ResultsOur analyses show that cultivated olives exhibit slightly lower levels of overall genetic diversity than wild forms, and that this can be partially explained by the occurrence of a mild population bottleneck 5000-7000 years ago during the primary domestication period. We also provide the first phylogenetic analysis of genome-wide sequences, which supports a continuous process of domestication of the olive tree. This, together with population structure and introgression analyses highlights genetic admixture with wild populations across the Mediterranean Basin in the course of domestication.ConclusionsAltogether, our results suggest that a primary domestication area in the eastern Mediterranean basin was followed by numerous secondary events across most countries of southern Europe and northern Africa, often involving genetic admixture with genetically rich wild populations, particularly from the western Mediterranean Basin. Based on selection tests and a search for selective sweeps, we found that genes associated with stress response and developmental processes were positively selected in cultivars. However, we did not find evidence that genes involved in fruit size or oil content were under positive selection.

It remains a major challenge to identify the genes and mutations that lead to plant sexual differentiation. Here, we study the structure and evolution of the sex-determining region (SDR) in Vitis species. We report an improved, chromosome-scale Cabernet Sauvignon genome sequence and the phased assembly of nine wild and cultivated grape genomes. By resolving twenty Vitis SDR haplotypes, we compare male, female, and hermaphrodite haplotype structures and identify sex-linked regions. Coupled with gene expression data, we identify a candidate male-sterility mutation in the VviINP1 gene and potential female-sterility function associated with the transcription factor VviYABBY3. Our data suggest that dioecy has been lost during domestication through a rare recombination event between male and female haplotypes. This work significantly advances the understanding of the genetic basis of sex determination in Vitis and provides the information necessary to rapidly identify sex types in grape breeding programs., Grapevine is one of a few ancestrally dioecious crops that are reverted to hermaphroditism during domestication. Here, the authors identify candidate genes related to male- and female-sterility in grapes and describe the genetic process that led to hermaphroditism during domestication.

Over two thousand plant species have been modified morphologically through cultivation and human use. Here, we review three aspects of crop domestication that are currently undergoing marked revisions, due to analytical advancements and their application to whole genome resequencing (WGS) data. We begin by discussing the duration and demographic history of domestication. There has been debate as to whether domestication occurred quickly or slowly. The latter is tentatively supported both by fossil data and application of WGS data to sequentially Markovian coalescent methods that infer the history of effective population size. This history suggests the possibility of extended human impacts on domesticated lineages prior to their purposeful cultivation. We also make the point that demographic history matters, because it shapes patterns and levels of extant genetic diversity. We illustrate this point by discussing the evolutionary processes that contribute to the empirical observation that most crops examined to date have more putatively deleterious alleles than their wild relatives. These deleterious alleles may contribute to genetic load within crops and may be fitting targets for crop improvement. Finally, the same demographic factors are likely to shape the spectrum of structural variants (SVs) within crops. SVs are known to underlie many of the phenotypic changes associated with domestication and crop improvement, but we currently lack sufficient knowledge about the mechanisms that create SVs, their rates of origin, their population frequencies and their phenotypic effects.

Transposable elements (TEs) compose the majority of angiosperm DNA. Plants counteract TE activity by silencing them epigenetically. One form of epigenetic silencing requires 21–22 nt small interfering RNAs that act to degrade TE mRNA and may also trigger DNA methylation. DNA methylation is reinforced by a second mechanism, the RNA-dependent DNA methylation (RdDM) pathway. RdDM relies on 24 nt small interfering RNAs and ultimately establishes TEs in a quiescent state. These host factors interact at a systems level, but there have been no system level analyses of their interactions. Here, we define a deterministic model that represents the propagation of active TEs, aspects of the host response and the accumulation of silenced TEs. We describe general properties of the model and also fit it to biological data in order to explore two questions. The first is why two overlapping pathways are maintained, given that both are likely energetically expensive. Under our model, RdDM silenced TEs effectively even when the initiation of silencing was weak. This relationship implies that only a small amount of RNAi is needed to initiate TE silencing, but reinforcement by RdDM is necessary to efficiently counter TE propagation. Second, we investigated the reliance of the host response on rates of TE deletion. The model predicted that low levels of deletion lead to few active TEs, suggesting that silencing is most efficient when methylated TEs are retained in the genome, thereby providing one explanation for the large size of plant genomes.

We gathered genomic data from grapes (Vitis vinifera ssp. vinifera), a clonally propagated perennial crop, to address three ongoing mysteries about plant domestication. The first is the duration of domestication; archaeological evidence suggests that domestication occurs over millennia, but genetic evidence indicates that it can occur rapidly. We estimated that our wild and cultivated grape samples diverged ∼22,000 years ago and that the cultivated lineage experienced a steady decline in population size (Ne ) thereafter. The long decline may reflect low-intensity management by humans before domestication. The second mystery is the identification of genes that contribute to domestication phenotypes. In cultivated grapes, we identified candidate-selected genes that function in sugar metabolism, flower development, and stress responses. In contrast, candidate-selected genes in the wild sample were limited to abiotic and biotic stress responses. A genomic region of high divergence corresponded to the sex determination region and included a candidate male sterility factor and additional genes with sex-specific expression. The third mystery concerns the cost of domestication. Annual crops accumulate putatively deleterious variants, in part due to strong domestication bottlenecks. The domestication of perennial crops differs from that of annuals in several ways, including the intensity of bottlenecks, and it is not yet clear if they accumulate deleterious variants. We found that grape accessions contained 5.2% more deleterious variants than wild individuals, and these were more often in a heterozygous state. Using forward simulations, we confirm that clonal propagation leads to the accumulation of recessive deleterious mutations but without decreasing fitness.

DNA methylation labels a specific subset of genes in plant genomes. Recent work has shown that this gene-body methylation (gbM) is a conserved feature of orthologs, because highly methylated genes in one species tend to be highly methylated in another. In this study, we examined the exceptions to that rule by identifying genes that differ in gbM status between two plant species-Arabidopsis thaliana and Arabidopsis lyrata. Using Capsella grandiflora as an outgroup, we polarized the loss and gain of gbM for orthologs in the Arabidopsis lineage. Our survey identified a few hundred genes that differed between ingroup species, out of ∼9,000 orthologs. The estimated rate of gbM gain was ∼2 × 10-9 per gene per year for both ingroup taxa and was similar to the loss rate in A. lyrata. In contrast, A. thaliana had a ∼3-fold higher estimated rate of gbM loss per gene, consistent with a recent diminishment of genome size. As in previous studies, we found that body-methylated genes were expressed broadly across tissues and were also longer than other genic sets. Genes that differed in gbM status exhibited higher variance in expression between species than genes that were body-methylated in both species. Moreover, the gain of gbM in one lineage tended to be associated with an increase of expression in that lineage. The genes that varied in gbM status between species varied more significantly in length between species than other sets of genes; we hypothesize that length is a key feature in the transition between body-methylated and nonmethylated genes.

Analysis of genomic and phenotypic data in Helianthus species demonstrates that large chromosomal regions contribute to multiple traits associated with distinct ecotypes.