Cycles of satellite and transposon evolution in Arabidopsis centromeres.

Centromeres are critical for cell division, loading CENH3 or CENPA histone variant nucleosomes, directing kinetochore formation and allowing chromosome segregation1,2. Despite their conserved function, centromere size and structure are diverse across species. To understand this centromere paradox3,4, it is necessary to know how centromeric diversity is generated and whether it reflects ancient trans-species variation or, instead, rapid post-speciation divergence. To address these questions, we assembled 346 centromeres from 66 Arabidopsis thaliana and 2 Arabidopsis lyrata accessions, which exhibited a remarkable degree of intra- and inter-species diversity. A. thaliana centromere repeat arrays are embedded in linkage blocks, despite ongoing internal satellite turnover, consistent with roles for unidirectional gene conversion or unequal crossover between sister chromatids in sequence diversification. Additionally, centrophilic ATHILA transposons have recently invaded the satellite arrays. To counter ATHILA invasion, chromosome-specific bursts of satellite homogenization generate higher-order repeats and purge transposons, in line with cycles of repeat evolution. Centromeric sequence changes are even more extreme in comparison between A. thaliana and A. lyrata. Together, our findings identify rapid cycles of transposon invasion and purging through satellite homogenization, which drive centromere evolution and ultimately contribute to speciation.

The Genetic Architecture of Adaptation to Leaf and Root Bacterial Microbiota in Arabidopsis thaliana.

Understanding the role of the host genome in modulating microbiota variation is a need to shed light on the holobiont theory and overcome the current limits on the description of host-microbiota interactions at the genomic and molecular levels. However, the host genetic architecture structuring microbiota is only partly described in plants. In addition, most association genetic studies on microbiota are often carried out outside the native habitats where the host evolves and the identification of signatures of local adaptation on the candidate genes has been overlooked. To fill these gaps and dissect the genetic architecture driving adaptive plant-microbiota interactions, we adopted a genome-environment association (GEA) analysis on 141 whole-genome sequenced natural populations of Arabidopsis thaliana characterized in situ for their leaf and root bacterial communities in fall and spring, and a large range of nonmicrobial ecological factors (i.e., climate, soil, and plant communities). A much higher fraction of among-population microbiota variance was explained by the host genetics than by nonmicrobial ecological factors. Importantly, the relative importance of host genetics and nonmicrobial ecological factors in explaining the presence of particular operational taxonomic units (OTUs) differs between bacterial families and genera. In addition, the polygenic architecture of adaptation to bacterial communities was highly flexible between plant compartments and seasons. Relatedly, signatures of local adaptation were stronger on quantitative trait loci (QTLs) of the root microbiota in spring. Finally, plant immunity appears as a major source of adaptive genetic variation structuring bacterial assemblages in A. thaliana.

Robustness of plant quantitative disease resistance is provided by a decentralized immune network.

Quantitative disease resistance (QDR) represents the predominant form of resistance in natural populations and crops. Surprisingly, very limited information exists on the biomolecular network of the signaling machineries underlying this form of plant immunity. This lack of information may result from its complex and quantitative nature. Here, we used an integrative approach including genomics, network reconstruction, and mutational analysis to identify and validate molecular networks that control QDR in Arabidopsis thaliana in response to the bacterial pathogen Xanthomonas campestris To tackle this challenge, we first performed a transcriptomic analysis focused on the early stages of infection and using transgenic lines deregulated for the expression of RKS1, a gene underlying a QTL conferring quantitative and broad-spectrum resistance to XcampestrisRKS1-dependent gene expression was shown to involve multiple cellular activities (signaling, transport, and metabolism processes), mainly distinct from effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses already characterized in Athaliana Protein-protein interaction network reconstitution then revealed a highly interconnected and distributed RKS1-dependent network, organized in five gene modules. Finally, knockout mutants for 41 genes belonging to the different functional modules of the network revealed that 76% of the genes and all gene modules participate partially in RKS1-mediated resistance. However, these functional modules exhibit differential robustness to genetic mutations, indicating that, within the decentralized structure of the QDR network, some modules are more resilient than others. In conclusion, our work sheds light on the complexity of QDR and provides comprehensive understanding of a QDR immune network.

Fight hard or die trying: when plants face pathogens under heat stress.

In their natural environment, plants are exposed to biotic or abiotic stresses that occur sequentially or simultaneously. Plant responses to these stresses have been studied widely and have been well characterised in simplified systems involving single plant species facing individual stress. Temperature elevation is a major abiotic driver of climate change and scenarios have predicted an increase in the number and severity of epidemics. In this context, here we review the available data on the effect of heat stress on plant-pathogen interactions. Considering 45 studies performed on model or crop species, we discuss the possible implications of the optimum growth temperature of plant hosts and pathogens, mode of stress application and temperature variation on resistance modulations. Alarmingly, most identified resistances are altered under temperature elevation, regardless of the plant and pathogen species. Therefore, we have listed current knowledge on heat-dependent plant immune mechanisms and pathogen thermosensory processes, mainly studied in animals and human pathogens, that could help to understand the outcome of plant-pathogen interactions under elevated temperatures. Based on a general overview of the mechanisms involved in plant responses to pathogens, and integrating multiple interactions with the biotic environment, we provide recommendations to optimise plant disease resistance under heat stress and to identify thermotolerant resistance mechanisms.

Two-way mixed-effects methods for joint association analysis using both host and pathogen genomes.

Infectious diseases are often affected by specific pairings of hosts and pathogens and therefore by both of their genomes. The integration of a pair of genomes into genome-wide association mapping can provide an exquisitely detailed view of the genetic landscape of complex traits. We present a statistical method, ATOMM (Analysis with a Two-Organism Mixed Model), that maps a trait of interest to a pair of genomes simultaneously; this method makes use of whole-genome sequence data for both host and pathogen organisms. ATOMM uses a two-way mixed-effect model to test for genetic associations and cross-species genetic interactions while accounting for sample structure including interactions between the genetic backgrounds of the two organisms. We demonstrate the applicability of ATOMM to a joint association study of quantitative disease resistance (QDR) in the Arabidopsis thaliana-Xanthomonas arboricola pathosystem. Our method uncovers a clear host-strain specificity in QDR and provides a powerful approach to identify genetic variants on both genomes that contribute to phenotypic variation.

HpaP Sequesters HrpJ, an Essential Component of Ralstonia solanacearum Virulence That Triggers Necrosis in Arabidopsis.

The Gram-negative bacterium Ralstonia solanacearum, the causal agent of bacterial wilt, is a worldwide major crop pathogen whose virulence strongly relies on a type III secretion system (T3SS). This extracellular apparatus allows the translocation of proteins, called type III effectors (T3Es), directly into the host cells. To date, very few data are available in plant-pathogenic bacteria concerning the role played by type III secretion (T3S) regulators at the posttranslational level. We have demonstrated that HpaP, a putative T3S substrate specificity switch protein of R. solanacearum, controls T3E secretion. To better understand the role of HpaP on T3S control, we analyzed the secretomes of the GMI1000 wild-type strain as well as the hpaP mutant using a mass spectrometry experiment (liquid chromatography tandem mass spectrometry). The secretomes of both strains appeared to be very similar and highlighted the modulation of the secretion of few type III substrates. Interestingly, only one type III-associated protein, HrpJ, was identified as specifically secreted by the hpaP mutant. HrpJ appeared to be an essential component of the T3SS, essential for T3S and pathogenicity. We further showed that HrpJ is specifically translocated in planta by the hpaP mutant and that HrpJ can physically interact with HpaP. Moreover, confocal microscopy experiments demonstrated a cytoplasmic localization for HrpJ once in planta. When injected into Arabidopsis thaliana leaves, HrpJ is able to trigger a necrosis on 16 natural accessions. A genome-wide association mapping revealed a major association peak with 12 highly significant single-nucleotide polymorphisms located on a plant acyl-transferase.

Adaptation to Plant Communities across the Genome of Arabidopsis thaliana.

Despite the importance of plant-plant interactions on plant community dynamics and crop yield, our understanding of the adaptive genetics underlying these interactions is still limited and deserves to be investigated in the context of complex and diffuse interactions occurring in plant assemblages. Here, based on 145 natural populations of Arabidopsis thaliana located in south-west of France and characterized for plant communities, we conducted a Genome-Environment Association analysis to finely map adaptive genomic regions of A. thaliana associated with plant community descriptors. To control for correlated abiotic environment effects, we also characterized the populations for a set of biologically meaningful climate and soil variables. A nonnegligible fraction of top single nucleotide polymorphisms was associated with both plant community descriptors and abiotic variables, highlighting the importance of considering the actual abiotic drivers of plant communities to disentangle genetic variants for biotic adaptation from genetic variants for abiotic adaptation. The adaptive loci associated with species abundance were highly dependent on the identity of the neighboring species suggesting a high degree of biotic specialization of A. thaliana to members of its plant interaction network. Moreover, the identification of adaptive loci associated with α-diversity and composition of plant communities supports the ability of A. thaliana to interact simultaneously with multiple plant neighbors, which in turn can help to understand the role of community-wide selection. Altogether, our study highlights that dissecting the genetic basis underlying plant-plant interactions at a regional scale while controlling for abiotic confounding factors can help understanding the adaptive mechanisms modulating natural plant assemblages.

The long-term maintenance of a resistance polymorphism through diffuse interactions.

Plant resistance (R) genes are a crucial component in plant defence against pathogens. Although R genes often fail to provide durable resistance in an agricultural context, they frequently persist as long-lived balanced polymorphisms in nature. Standard theory explains the maintenance of such polymorphisms through a balance of the costs and benefits of resistance and virulence in a tightly coevolving host-pathogen pair. However, many plant-pathogen interactions lack such specificity. Whether, and how, balanced polymorphisms are maintained in diffusely interacting species is unknown. Here we identify a naturally interacting R gene and effector pair in Arabidopsis thaliana and its facultative plant pathogen, Pseudomonas syringae. The protein encoded by the R gene RPS5 recognizes an AvrPphB homologue (AvrPphB2) and exhibits a balanced polymorphism that has been maintained for over 2 million years (ref. 3). Consistent with the presence of an ancient balanced polymorphism, the R gene confers a benefit when plants are infected with P. syringae carrying avrPphB2 but also incurs a large cost in the absence of infection. RPS5 alleles are maintained at intermediate frequencies in populations globally, suggesting ubiquitous selection for resistance. However, the presence of P. syringae carrying avrPphB is probably insufficient to explain the RPS5 polymorphism. First, avrPphB homologues occur at very low frequencies in P. syringae populations on A. thaliana. Second, AvrPphB only rarely confers a virulence benefit to P. syringae on A. thaliana. Instead, we find evidence that selection for RPS5 involves multiple non-homologous effectors and multiple pathogen species. These results and an associated model suggest that the R gene polymorphism in A. thaliana may not be maintained through a tightly coupled interaction involving a single coevolved R gene and effector pair. More likely, the stable polymorphism is maintained through complex and diffuse community-wide interactions.

The genetics underlying natural variation of plant-plant interactions, a beloved but forgotten member of the family of biotic interactions.

Despite the importance of plant-plant interactions on crop yield and plant community dynamics, our understanding of the genetic and molecular bases underlying natural variation of plant-plant interactions is largely limited in comparison with other types of biotic interactions. By listing 63 quantitative trait loci (QTL) mapping and global gene expression studies based on plants directly challenged by other plants, we explored whether the genetic architecture and the function of the candidate genes underlying natural plant-plant interactions depend on the type of interactions between two plants (competition versus commensalism versus reciprocal helping versus asymmetry). The 16 transcriptomic studies are unevenly distributed between competitive interactions (n = 12) and asymmetric interactions (n = 4, all focusing on response to parasitic plants). By contrast, 17 and 30 QTL studies were identified for competitive interactions and asymmetric interactions (either weed suppressive ability or response to parasitic plants), respectively. Surprisingly, no studies have been carried out on the identification of genetic and molecular bases underlying natural variation in positive interactions. The candidate genes underlying natural plant-plant interactions can be classified into seven categories of plant function that have been identified in artificial environments simulating plant-plant interactions either frequently (photosynthesis, hormones), only recently (cell wall modification and degradation, defense pathways against pathogens) or rarely (ABC transporters, histone modification and meristem identity/life history traits). Finally, we introduce several avenues that need to be explored in the future to obtain a thorough understanding of the genetic and molecular bases underlying plant-plant interactions within the context of realistic community complexity.

Madeiran Arabidopsis thaliana Reveals Ancient Long-Range Colonization and Clarifies Demography in Eurasia.

The study of model organisms on islands may shed light on rare long-range dispersal events, uncover signatures of local evolutionary processes, and inform demographic inference on the mainland. Here, we sequenced the genomes of Arabidopsis thaliana samples from the oceanic island of Madeira. These samples include the most diverged worldwide, likely a result of long isolation on the island. We infer that colonization of Madeira happened between 70 and 85 ka, consistent with a propagule dispersal model (of size ≥10), or with an ecological window of opportunity. This represents a clear example of a natural long-range dispersal event in A. thaliana. Long-term effective population size on the island, rather than the founder effect, had the greatest impact on levels of diversity, and rates of coalescence. Our results uncover a selective sweep signature on the ancestral haplotype of a known translocation in Eurasia, as well as the possible importance of the low phosphorous availability in volcanic soils, and altitude, in shaping early adaptations to the island conditions. Madeiran genomes, sheltered from the complexities of continental demography, help illuminate ancient demographic events in Eurasia. Our data support a model in which two separate lineages of A. thaliana, one originating in Africa and the other from the Caucasus expanded and met in Iberia, resulting in a secondary contact zone there. Although previous studies inferred that the westward expansion of A. thaliana coincided with the spread of human agriculture, our results suggest that it happened much earlier (20-40 ka).

Genome-wide association study reveals new loci involved in Arabidopsis thaliana and Turnip mosaic virus (TuMV) interactions in the field.

The genetic architecture of plant response to viruses has often been studied in model nonnatural pathosystems under controlled conditions. There is an urgent need to elucidate the genetic architecture of the response to viruses in a natural setting. A field experiment was performed in each of two years. In total, 317 Arabidopsis thaliana accessions were inoculated with its natural Turnip mosaic virus (TuMV). The accessions were phenotyped for viral accumulation, frequency of infected plants, stem length and symptoms. Genome-wide association mapping was performed. Arabidopsis thaliana exhibits extensive natural variation in its response to TuMV in the field. The underlying genetic architecture reveals a more quantitative picture than in controlled conditions. Ten genomic regions were consistently identified across the two years. RTM3 (Restricted TEV Movement 3) is a major candidate for the response to TuMV in the field. New candidate genes include Dead box helicase 1, a Tim Barrel domain protein and the eukaryotic translation initiation factor eIF3b. To our knowledge, this study is the first to report the genetic architecture of quantitative response of A. thaliana to a naturally occurring virus in a field environment, thereby highlighting relevant candidate genes involved in plant virus interactions in nature.

Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field.

Although the contribution of cytonuclear interactions to plant fitness variation is relatively well documented at the interspecific level, the prevalence of cytonuclear interactions at the intraspecific level remains poorly investigated. In this study, we set up a field experiment to explore the range of effects that cytonuclear interactions have on fitness-related traits in Arabidopsis thaliana To do so, we created a unique series of 56 cytolines resulting from cytoplasmic substitutions among eight natural accessions reflecting within-species genetic diversity. An assessment of these cytolines and their parental lines scored for 28 adaptive whole-organism phenotypes showed that a large proportion of phenotypic traits (23 of 28) were affected by cytonuclear interactions. The effects of these interactions varied from slight but frequent across cytolines to strong in some specific parental pairs. Two parental pairs accounted for half of the significant pairwise interactions. In one parental pair, Ct-1/Sha, we observed symmetrical phenotypic responses between the two nuclear backgrounds when combined with specific cytoplasms, suggesting nuclear differentiation at loci involved in cytonuclear epistasis. In contrast, asymmetrical phenotypic responses were observed in another parental pair, Cvi-0/Sha. In the Cvi-0 nuclear background, fecundity and phenology-related traits were strongly affected by the Sha cytoplasm, leading to a modified reproductive strategy without penalizing total seed production. These results indicate that natural variation in cytoplasmic and nuclear genomes interact to shape integrative traits that contribute to adaptation, thereby suggesting that cytonuclear interactions can play a major role in the evolutionary dynamics ofA. thaliana.

Coselected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana.

The "mustard oil bomb" is a major defense mechanism in the Brassicaceae, which includes crops such as canola and the model plant Arabidopsis thaliana. These plants produce and store blends of amino acid-derived secondary metabolites called glucosinolates. Upon tissue rupture by natural enemies, the myrosinase enzyme hydrolyses glucosinolates, releasing defense molecules. Brassicaceae display extensive variation in the mixture of glucosinolates that they produce. To investigate the genetics underlying natural variation in glucosinolate profiles, we conducted a large genome-wide association study of 22 methionine-derived glucosinolates using A. thaliana accessions from across Europe. We found that 36% of among accession variation in overall glucosinolate profile was explained by genetic differentiation at only three known loci from the glucosinolate pathway. Glucosinolate-related SNPs were up to 490-fold enriched in the extreme tail of the genome-wide [Formula: see text] scan, indicating strong selection on loci controlling this pathway. Glucosinolate profiles displayed a striking longitudinal gradient with alkenyl and hydroxyalkenyl glucosinolates enriched in the West. We detected a significant contribution of glucosinolate loci toward general herbivore resistance and lifetime fitness in common garden experiments conducted in France, where accessions are enriched in hydroxyalkenyls. In addition to demonstrating the adaptive value of glucosinolate profile variation, we also detected long-distance linkage disequilibrium at two underlying loci, GS-OH and GS-ELONG. Locally cooccurring alleles at these loci display epistatic effects on herbivore resistance and fitness in ecologically realistic conditions. Together, our results suggest that natural selection has favored a locally adaptive configuration of physically unlinked loci in Western Europe.

Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana.

A major challenge in evolutionary biology and plant breeding is to identify the genetic basis of complex quantitative traits, including those that contribute to adaptive variation. Here we review the development of new methods and resources to fine-map intraspecific genetic variation that underlies natural phenotypic variation in plants. In particular, the analysis of 107 quantitative traits reported in the first genome-wide association mapping study in Arabidopsis thaliana sets the stage for an exciting time in our understanding of plant adaptation. We also argue for the need to place phenotype-genotype association studies in an ecological context if one is to predict the evolutionary trajectories of plant species.

Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines.

Although pioneered by human geneticists as a potential solution to the challenging problem of finding the genetic basis of common human diseases, genome-wide association (GWA) studies have, owing to advances in genotyping and sequencing technology, become an obvious general approach for studying the genetics of natural variation and traits of agricultural importance. They are particularly useful when inbred lines are available, because once these lines have been genotyped they can be phenotyped multiple times, making it possible (as well as extremely cost effective) to study many different traits in many different environments, while replicating the phenotypic measurements to reduce environmental noise. Here we demonstrate the power of this approach by carrying out a GWA study of 107 phenotypes in Arabidopsis thaliana, a widely distributed, predominantly self-fertilizing model plant known to harbour considerable genetic variation for many adaptively important traits. Our results are dramatically different from those of human GWA studies, in that we identify many common alleles of major effect, but they are also, in many cases, harder to interpret because confounding by complex genetics and population structure make it difficult to distinguish true associations from false. However, a-priori candidates are significantly over-represented among these associations as well, making many of them excellent candidates for follow-up experiments. Our study demonstrates the feasibility of GWA studies in A. thaliana and suggests that the approach will be appropriate for many other organisms.

An atypical kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis.

The failure of gene-for-gene resistance traits to provide durable and broad-spectrum resistance in an agricultural context has led to the search for genes underlying quantitative resistance in plants. Such genes have been identified in only a few cases, all for fungal or nematode resistance, and encode diverse molecular functions. However, an understanding of the molecular mechanisms of quantitative resistance variation to other enemies and the associated evolutionary forces shaping this variation remain largely unknown. We report the identification, map-based cloning and functional validation of QRX3 (RKS1, Resistance related KinaSe 1), conferring broad-spectrum resistance to Xanthomonas campestris (Xc), a devastating worldwide bacterial vascular pathogen of crucifers. RKS1 encodes an atypical kinase that mediates a quantitative resistance mechanism in plants by restricting bacterial spread from the infection site. Nested Genome-Wide Association mapping revealed a major locus corresponding to an allelic series at RKS1 at the species level. An association between variation in resistance and RKS1 transcription was found using various transgenic lines as well as in natural accessions, suggesting that regulation of RKS1 expression is a major component of quantitative resistance to Xc. The co-existence of long lived RKS1 haplotypes in A. thaliana is shared with a variety of genes involved in pathogen recognition, suggesting common selective pressures. The identification of RKS1 constitutes a starting point for deciphering the mechanisms underlying broad spectrum quantitative disease resistance that is effective against a devastating and vascular crop pathogen. Because putative RKS1 orthologous have been found in other Brassica species, RKS1 provides an exciting opportunity for plant breeders to improve resistance to black rot in crops.

Genome wide association study of Arabidopsis seed mucilage layers at a regional scale.

The myxospermous species Arabidopsis thaliana extrudes a polysaccharidic mucilage from the seed coat epidermis during imbibition. The whole seed mucilage can be divided into a seed-adherent layer and a fully soluble layer, both layers presenting natural genetic variations. The adherent mucilage is variable in size and composition, while the soluble mucilage is variable in composition and physical properties. Studies reporting both the genetic architecture and the putative selective agents acting on this natural genetic variation are scarce. In this study, we set up a Genome Wide Association study (GWAS) based on 424 natural accessions collected from 166 natural populations of A. thaliana located south-west of France and previously characterized for a very important number of abiotic and biotic factors. We identified an extensive genetic variation for both mucilage layers. The adherent mucilage was mainly related to precipitation and temperature whereas the non-adherent mucilage was unrelated to any environmental factors. By combining a hierarchical Bayesian model with a local score approach, we identified 55 and 28 candidate genes, corresponding to 26 and 10 QTLs for the adherent and non-adherent mucilages, respectively. Putative or characterized function and expression data available in the literature were used to filter the candidate genes. Only one gene among our set of candidate genes was already described as a seed mucilage actor, leaving a large set of new candidates putatively implicated inseed mucilage synthesis or release. The present study lay out foundation to understand the influence of regional ecological factors acting on seed mucilage in A. thaliana.

Natural genetic variation underlying the negative effect of elevated CO2 on ionome composition in Arabidopsis thaliana.

The elevation of atmospheric CO2 leads to a decline in plant mineral content, which might pose a significant threat to food security in coming decades. Although few genes have been identified for the negative effect of elevated CO2 on plant mineral composition, several studies suggest the existence of genetic factors. Here, we performed a large-scale study to explore genetic diversity of plant ionome responses to elevated CO2, using six hundred Arabidopsis thaliana accessions, representing geographical distributions ranging from worldwide to regional and local environments. We show that growth under elevated CO2 leads to a global decrease of ionome content, whatever the geographic distribution of the population. We observed a high range of genetic diversity, ranging from the most negative effect to resilience or even to a benefit in response to elevated CO2. Using genome-wide association mapping, we identified a large set of genes associated with this response, and we demonstrated that the function of one of these genes is involved in the negative effect of elevated CO2 on plant mineral composition. This resource will contribute to understand the mechanisms underlying the effect of elevated CO2 on plant mineral nutrition, and could help towards the development of crops adapted to a high-CO2 world.

A pan-genome of 69 Arabidopsis thaliana accessions reveals a conserved genome structure throughout the global species range.

Although originally primarily a system for functional biology, Arabidopsis thaliana has, owing to its broad geographical distribution and adaptation to diverse environments, developed into a powerful model in population genomics. Here we present chromosome-level genome assemblies of 69 accessions from a global species range. We found that genomic colinearity is very conserved, even among geographically and genetically distant accessions. Along chromosome arms, megabase-scale rearrangements are rare and typically present only in a single accession. This indicates that the karyotype is quasi-fixed and that rearrangements in chromosome arms are counter-selected. Centromeric regions display higher structural dynamics, and divergences in core centromeres account for most of the genome size variations. Pan-genome analyses uncovered 32,986 distinct gene families, 60% being present in all accessions and 40% appearing to be dispensable, including 18% private to a single accession, indicating unexplored genic diversity. These 69 new Arabidopsis thaliana genome assemblies will empower future genetic research.

The genetic architecture of repeated local adaptation to climate in distantly related plants.

Closely related species often use the same genes to adapt to similar environments. However, we know little about why such genes possess increased adaptive potential and whether this is conserved across deeper evolutionary lineages. Adaptation to climate presents a natural laboratory to test these ideas, as even distantly related species must contend with similar stresses. Here, we re-analyse genomic data from thousands of individuals from 25 plant species as diverged as lodgepole pine and Arabidopsis (~300 Myr). We test for genetic repeatability based on within-species associations between allele frequencies in genes and variation in 21 climate variables. Our results demonstrate significant statistical evidence for genetic repeatability across deep time that is not expected under randomness, identifying a suite of 108 gene families (orthogroups) and gene functions that repeatedly drive local adaptation to climate. This set includes many orthogroups with well-known functions in abiotic stress response. Using gene co-expression networks to quantify pleiotropy, we find that orthogroups with stronger evidence for repeatability exhibit greater network centrality and broader expression across tissues (higher pleiotropy), contrary to the 'cost of complexity' theory. These gene families may be important in helping wild and crop species cope with future climate change, representing important candidates for future study.