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Venon, A.

Publications and source records attributed to Venon, A..

13 recordsLinked to original sources

Genomic forecasting links climate-associated variation to spring phenology in the European wild apple, a crop wild relative of the cultivated apple

Climate-associated genomic variation is often used as a proxy for adaptive potential, yet whether it reflects adaptation with phenotypic consequences, rather than demography alone, is rarely tested in long-lived species. Genomic offsets forecast climate maladaptation from genotype-environment models but are seldom validated against phenotypes. We combined whole-genome resequencing, SNP and transposable element insertion polymorphism (TIP) variation, landscape genomics, genome-wide association, genomic offset, and common-garden phenotyping in the European wild apple (Malus sylvestris Mill.), a crop wild relative with a complex demographic history, to test this. Results: Of 148 resequenced accessions (135 wild, 13 cultivated), 89 wild individuals formed the core dataset. Population structure was associated with Last Glacial Maximum precipitation rather than contemporary climate, and genetic diversity increased from west to east. Genome-environment associations across 9.75 million SNPs identified climate-associated loci enriched in photoperiod-related flowering-time genes, with limited overlap with phenotype-associated loci. SNP-based genomic offset was associated with bud-break timing in the Saclay common garden (marginal R2 = 0.31), with higher offsets corresponding to earlier bud break, but not with growth or ecophysiological traits. This association depended on Austrian and Romanian populations and was clearest in non-admixed wild individuals. Offsets based on TIPs or glacial climate did not predict measured phenotypes. Conclusions: Climate association, phenotypic relevance, and predictive power of genomic variation are separable. In a long-lived tree, genomic offset predicted spring phenology, a key adaptive trait, but this signal varied across provenances and ancestries and was absent for transposable elements. Genomic offsets can therefore forecast potential phenological maladaptation, provided they are validated against phenotypes such as bud break.

ecology↗

Domestication altered defense responses and host-aphid interaction networks in apples

- Domestication can profoundly reshape plant defense strategies and host-parasite interactions, but its consequences for resistance and coevolution in perennial crops remain poorly understood. We investigated how domestication altered apple responses to its major pest, the rosy apple aphid (Dysaphis plantaginea). - We compared wild (Malus orientalis, two geographically differentiated M. sylvestris populations) and cultivated (cider and dessert M. domestica) apple genotypes against two genetically distinct aphid genotypes, combining controlled infestation experiments with phenotypic measurements, paired host-aphid RNA-seq, co-expression network analysis, and genome-wide selection scans. - Aphid fitness and host resistance varied strongly across host populations: domesticated apples supported higher aphid performance, whereas Romanian M. sylvestris showed the highest resistance, revealing marked host-aphid genotype-specific asymmetric compatibility. Cultivated apples have developed extensive inducible transcriptional defense responses, whereas wild populations showed weaker perturbation despite lower aphid fitness, consistent with more constitutive defense. Host-aphid co-expression analyses identified candidate coevolutionary modules linking host resistance genes under balancing selection with aphid genes under positive selection. - Together, these results demonstrate that apple domestication reshaped defense-associated regulatory networks and modified the adaptive landscape experienced by aphid populations, providing new insight into the evolutionary consequences of perennial crop domestication on host-parasite interactions.

evolutionary biology↗

How to be dispensable: genomic and transcriptomic determinants in maize genes

BackgroundPlant genomes harbour a substantial proportion of dispensable genes - present only in a subset of individuals - that differ from ubiquitously shared core genes in multiple genomic and expression features. While these differences have been repeatedly documented, the factors shaping gene dispensability remain poorly understood. ResultsWe assembled a pan-gene set from eight maize inbred lines from American and European germplasms, together with their transcriptomic profile across 22 tissues/conditions, revealing the genomic and transcriptomic determinants of maize gene dispensability. Multivariate analysis demonstrates that gene expression level and purifying selection - rather than gene size - are the primary factors distinguishing core from dispensable genes. Dispensable genes overlap Helitrons at 4.6 times the rate of core genes, implicating Helitron-mediated gene capture as a major mechanism of dispensable gene formation. Classifying genes into stably expressed, variably expressed, and on-off categories shows that all three classes contain dispensable genes, though in different proportions than for core genes. Contrary to previous assumptions, we show that dispensable genes can participate in basal biological functions just as core genes, and that gene duplication likely provides only a partial mechanism for functional complementation of accessory genes absence. ConclusionsOur results provide novel insights into the molecular and evolutionary factors distinguishing core from dispensable genes and into the biological mechanisms shaping gene dispensability in maize, and demonstrate that classifying genes by transcriptional patterns provides a powerful framework for understanding the biological functions and evolutionary dynamics of both core and dispensable genes.

plant biology↗

Response to divergent selection on meiotic recombination in Saccharomyces cerevisiae

Meiotic recombination is a key driver of evolution in sexually reproducing species, reshaping genetic diversity by generating novel allelic combinations. The rate of recombination varies substantially across living organisms depending on cis- or trans-acting genetic elements, as seen in many species, including the yeast Saccharomyces cerevisiae. Here, we report on an experimental evolution-based study to better understand the factors shaping this natural variation. Starting with a genetically diverse population of S. cerevisiae, we have carried out recurrent divergent selection on recombination rate using a fluorescence-based sorting approach in four independent lineages. After ten generations, we observed an average response of recombination rate of +28% after positive selection and -24% after negative selection, within the interval used for selection. In the adjacent region, however, we observed a weaker response in the opposite direction, and no response in four other unlinked genomic regions. Whole-genome sequencing of individuals selected for high recombination revealed mixed outcomes in the four independently evolved lineages for high genome-wide recombination rates. However, all four lineages showed selection for high recombination locally, with particular haplotypes heavily favored and sequence- or structural variation-based heterozygosity selected against within the selection interval. Overall, this experimental evolution approach provides original and useful insights into the evolvability of the meiotic recombination rate and the associated genetic determinants.

genetics↗

Climate drives plasticity and genetic adaptation in apple trees

BackgroundPerennial crops respond to climate change through phenotypic plasticity and local adaptation, yet how these responses are orchestrated at the molecular level and reshaped by domestication remains poorly understood. ResultsWe grew 1,249 seedlings from five populations of M. domestica, M. orientalis, and M. sylvestris under four simulated European climates, quantified 12 phenotypic traits, performed RNA sequencing on 96 individuals, and integrated these data with previously published genome-wide polymorphism data from M. sylvestris to disentangle conserved climate responses from local adaptation. Climate was the dominant driver of phenotypic and transcriptional variation, revealing 344 conserved climate-responsive genes enriched for stress responses, nutrient metabolism, and cell wall biosynthesis. These genes are under strong purifying selection and carry fewer deleterious mutations. In contrast, genome-environment association analyses identified 217 loci associated with temperature and precipitation gradients, only a subset of which showed climate-responsive expression and elevated genomic differentiation. Population-level expression divergence closely mirrored neutral genetic differentiation, indicating that most transcriptomic divergence reflects demographic history rather than adaptive regulatory evolution. Domestication reshaped molecular diversity and mutation load without disrupting the conserved climate-response program. ConclusionsClimate responses in apple are primarily mediated by an evolutionarily conserved transcriptional program maintained by strong purifying selection, whereas local adaptation relies on largely distinct, population-specific loci. These findings reveal that conserved plasticity constitutes the dominant molecular response to climatic variation, whereas local adaptation contributes a secondary, population-specific layer of evolutionary change.

evolutionary biology↗

Genomic architecture of the self-incompatibility locus in apple provides insights into the evolution of collaborative non-self recognition

Self-incompatibility (SI) systems prevent self-fertilization, thereby maintaining genetic diversity in flowering plants. Among them, collaborative non-self recognition (CNSR) is the most widespread, yet the genomic organization and evolutionary maintenance of its multigenic recognition system remain poorly understood. Using 27 haplotype-resolved genomes from wild and domesticated apples (Malus spp.), we dissected the structure and evolution of the S-locus. We identified 17 S-RNase alleles and 500 pollen-expressed S-locus F-box brother (SFBB) genes across 18 families. The S-locus shows extensive structural divergence among alleles and transposable element accumulation, consistent with long-term restricted effective recombination. Despite this divergence, haplotypes carrying the same S-RNase allele retain remarkably conserved SFBB repertoires and gene organization, even across species boundaries, indicating that long-term balancing selection preserves highly conserved S-haplotype architectures associated with specific S-RNase lineages. Tandem duplication, positive selection, and signatures consistent with gene conversion contribute to the diversification of pollen-expressed SFBB genes while S-RNase-associated SFBB repertoires remain conserved across haplotypes carrying the same S-RNase allele. Our results reveal how a structurally dynamic yet evolutionarily constrained genomic region can sustain long-term S-allele diversity and preserve complex multigenic haplotype architectures in flowering plants.

genomics↗

Gene flow from the European wild apple and selection shaped the domesticated apple (Malus domestica Borkh.) genome

How selection and demography shape genomes of long-lived crops remains largely unresolved. Using apple (Malus domestica) as a model, we integrate 218 whole genomes (68 cultivated dessert/cider; 150 wild: M. sieversii, M. orientalis, M. sylvestris), RNA-seq, and a flowering-time GWAS to resolve how these forces forged the cultivated apple genome. Despite weak neutral differentiation and widespread admixture, dessert and cider apples form distinct gene pools that derive primarily from M. sieversii-M. orientalis rather than European M. sylvestris. We find no evidence of a strong domestication bottleneck, as expected in perennials. Demography-aware selection scans reveal largely non-overlapping targets: dessert shows more hard sweeps at genes linked to fruit quality, disease resistance, and flowering, whereas cider shows proportionally more soft sweeps and balancing selection; RNA-seq differential expression supports these candidates. Wild-to-crop introgression from M. sylvestris is extensive but heterogeneous by context: some introgressed tracts concentrate in hard-sweep regions and approach fixation (consistent with rapid, targeted uptake), whereas others persist at intermediate frequencies with soft-sweep signatures (consistent with diffuse, recurrent introgression of adaptive alleles). Extending to the phenotype, the lead chromosome 9 flowering-time association lies within an introgressed segment near a transposable element and is separated from sweep peaks, consistent with regulatory/polygenic control. Cultivated apples carry a lower predicted deleterious load than wild relatives. Together, these results provide one of the most comprehensive population genomic portraits of a perennial fruit tree domestication, clarifying how selection and adaptive introgression jointly shaped the cultivated apple genome architecture and yielding actionable targets for breeding and conservation. Significance statementPerennial crops are underexplored compared to annuals, leaving open the question of how selection, gene flow, and demography shape their genomes. Using the apple tree (Malus domestica), we analyzed 218 genomes, along with expression and trait data. Despite weak genome-wide differences, dessert and cider apples form distinct gene pools. Widespread gene flow from the European wild apple supplied adaptive alleles, with contrasting dynamics: in cider, a few introgressed DNA segments rose rapidly; in dessert, many variants shifted gradually. Cultivated apples also carry a lower predicted burden of harmful mutations than wild relatives. Together, these results redefine perennial domestication and pinpoint genomic targets to accelerate breeding and conservation.

genetics↗

Genomic footprints of domestication in almond (Prunus dulcis)

The domestication of perennial crops in the Mediterranean Basin remains unclear, particularly regarding the genomic consequences of human-mediated demographic shifts and selection. We analyzed 8.1 million single nucleotide polymorphisms from 96 cultivated almond (Prunus dulcis) accessions from Europe, North America, Central Asia, and New Zealand, alongside four wild relatives. Population structure analyses revealed four geographically differentiated cultivated groups (Central Asian, North American, and two European) and three wild populations (P. spinosissima, P. orientalis, and P. fenzliana). Cultivated almonds retained high genetic diversity, consistent with weak domestication bottlenecks typical of outcrossing perennials. Elevated diversity and private allele counts in Central Asian cultivars, with limited gene flow, support this region as an independent cradle of domestication. In contrast, extensive wild-to-crop gene flow--especially involving P. orientalis--has shaped the genomes of European and North American almonds. Genome-wide scans for selective sweeps showed most candidate genes under selection were population-specific, though often associated with similar biological functions, including stress responses and agronomic traits. This suggests repeated targeting of comparable pathways during domestication, despite distinct selection histories. Several selected genes in cultivated populations overlapped with those in wild relatives, particularly P. orientalis. Combined with demographic inferences indicating wild populations persistence through past climate fluctuations, these findings suggest wild gene pools retain adaptive alleles--either ancestrally shared or introgressed--that contributed to cultivated diversity. Altogether, our results reveal a complex, multi-regional domestication history for almonds, shaped by gene flow and recurrent selection. This study emphasizes wild relatives as adaptive diversity sources and reveals genomic bases of perennial crop evolution.

genomics↗

Sequential colonization events with restricted gene flow in a widespread European carnation species

The key questions relating to the evolutionary processes underlying plant colonization success pertain to the geographic origin of the source population(s), the location of the migration routes, the extent to which genetic diversity is reduced via founder effects, and the extent of gene flow among populations during expansion. However, these questions must still be addressed for perennial herbaceous plants with large geographic distributions. We investigated the colonization history of Dianthus carthusianorum (the Carthusian Pink), one of the most widespread European carnation species. We called genome-wide 236,964 SNPs from a large sample across the D. carthusianorum distribution range, and used up-to-date population genomics approaches (approximate Bayesian computation Random-Forest method, ABC-RF) to infer population demographic history. Spatial genetic structure and diversity analyses and demographic inferences indicated successive East-West colonization events by the Carthusian Pink. ABC-RF also revealed gene flow during colonization, but only among geographically close populations. This study provides important insights into the colonization processes of herbaceous perennial species belonging to one of Europes most diverse plant genera.

evolutionary biology↗

An additional area of apple domestication with crop-wild gene flow, and also cultivation of the local wild apple, in the Caucasus

Anthropogenic and natural divergence processes remain poorly studied in crop-wild fruit tree complexes, especially in the Caucasus, a pivotal region for plant domestication. We investigated anthropogenic and natural divergence processes in apples in the Caucasus using 26 microsatellite markers amplified in 550 wild and cultivated samples. We found two genetically distinct cultivated populations in Iran that are differentiated from Malus domestica, the standard cultivated apple worldwide. Coalescent-based inferences showed that these two cultivated populations originated from specific domestication events of M. orientalis in Iran. One of the Iranian clusters comprised both cultivated and forest trees, suggesting that either farmers use local wild apple for cultivation or that some forest trees are feral cultivars. We found evidence of substantial wild-crop and crop-crop gene flow in the Caucasus, as has been described in apple in Europe. In the Caucasus, we identified seven genetically differentiated populations of wild apple (Malus orientalis). Niche modeling combined with genetic diversity estimates indicated that these populations likely resulted from range changes during past glaciations. This study identifies Iran as a key region in the domestication of apple and M. orientalis as an additional contributor to the cultivated apple gene pool. Domestication of the apple tree therefore involved multiple origins of domestication in different geographic locations and substantial crop-wild hybridization, as found in other fruit trees. This study also highlights the impact of climate change on the natural divergence of a wild fruit tree and provides a starting point for apple conservation and breeding programs in the Caucasus.

evolutionary biology↗

Large-scale geographic survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa

AO_SCPLOWBSTRACTC_SCPLOWWith frequent host shifts involving the colonization of new hosts across large geographical ranges, crop pests are good models for examining the mechanisms of rapid colonization. The microbial partners of pest insects may also be involved in or affected by colonization processes, which has been little studied so far. We investigated the demographic history of the rosy apple aphid, Dysaphis plantaginea, a major pest of the cultivated apple (Malus domestica) in Europe, North Africa and North America, as well as the diversity of its microbiota. We genotyped a comprehensive sample of 714 colonies from Europe, Morocco and the US using mitochondrial (CytB and CO1), bacterial (16s rRNA and TrnpB), and 30 microsatellite markers. We detected five populations spread across the US, Morocco, Western and Eastern Europe and Spain. Populations showed weak genetic differentiation and high genetic diversity, except the ones from Morocco and North America that are likely the result of recent colonization events. Coalescent-based inferences revealed high levels of gene flow among populations during the colonization but did not allow determining the sequence of colonization of Europe, North America and Morroco by D. plantaginea, likely because of the weak genetic differentiation and the occurrence of gene flow among populations. We found that D. plantaginea rarely hosts other endosymbiotic bacteria than its obligate nutritional symbiont Buchnera aphidicola. This suggests that secondary endosymbionts did not play an important role in the rapid spread of the rosy apple aphid. These findings have fundamental importance for understanding pest colonization processes and implications for sustainable pest control programs.

evolutionary biology↗

Identification of key tissue-specific, biological processes by integrating enhancer information in maize gene regulatory networks

Enhancers are important regulators of gene expression during numerous crucial processes including tissue differentiation across development. In plants, their recent molecular characterization revealed their capacity to activate the expression of several target genes through the binding of transcription factors. Nevertheless, identifying these target genes at a genome-wide level remains a challenge, in particular in species with large genomes, where enhancers and target genes can be hundreds of kilobases away. Therefore, the contribution of enhancers to regulatory network is still poorly understood in plants. In this study, we investigate the enhancer-driven regulatory network of two maize tissues at different stages: leaves at seedling stage and husks (bracts) at flowering. Using a systems biology approach, we integrate genomic, epigenomic and transcriptomic data to model the regulatory relationship between transcription factors and their potential target genes. We identify regulatory modules specific to husk and V2-IST, and show that they are involved in distinct functions related to the biology of each tissue. We evidence enhancers exhibiting binding sites for two distinct transcription factor families (DOF and AP2/ERF) that drive the tissue-specificity of gene expression in seedling immature leaf and husk. Analysis of the corresponding enhancer sequences reveals that two different transposable element families (TIR transposon Mutator and MITE Pif/Harbinger) have shaped the regulatory network in each tissue, and that MITEs have provided new transcription factor binding sites that are involved in husk tissue-specificity.Significance Enhancers play a major role in regulating tissue-specific gene expression in higher eukaryotes, including angiosperms. While molecular characterization of enhancers has improved over the past years, identifying their target genes at the genome-wide scale remains challenging. Here, we integrate genomic, epigenomic and transcriptomic data to decipher the tissue-specific gene regulatory network controlled by enhancers at two different stages of maize leaf development. Using a systems biology approach, we identify transcription factor families regulating gene tissue-specific expression in husk and seedling leaves, and characterize the enhancers likely to be involved. We show that a large part of maize enhancers is derived from transposable elements, which can provide novel transcription factor binding sites crucial to the regulation of tissue-specific biological functions.Competing Interest StatementThe authors have declared no competing interest.View Full Text

systems biology↗

Genomic footprints of local adaptation along elevation gradients associate with present phenotypic variation in teosintes

Local adaptation across species range is widespread. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Because elevation gradients display continuous environmental changes at a short geographical scale, they provide an exceptional opportunity to investigate these questions. Here, we used two common gardens to phenotype 1664 plants from 11 populations of annual teosintes. These populations were sampled across two elevation gradients in Mexico. Our results point to a syndrome of adaptation to altitude with the production of offspring that flowered earlier, produced less tillers, and larger, longer and heavier grains with increasing elevation. We genotyped these plants for 178 outlier single nucleotide polymorphisms (SNPs), which had been chosen because they displayed excess of allele differentiation and/or correlation with environmental variables in six populations with contrasted altitudes. A high proportion of outlier SNPs associated with the phenotypic variation of at least one trait. We tested phenotypic pairwise correlations between traits, and found that the higher the correlation, the greater the number of common associated SNPs. In addition, allele frequencies at 87 of the outlier SNPs correlated with an environmental component best summarized by altitudinal variation on a broad sample of 28 populations. Chromosomal inversions were enriched for both phenotypically-associated and environmentally-correlated SNPs. Altogether, our results are consistent with the set-up of an altitudinal syndrome promoted by local adaptation of teosinte populations in the face of gene flow. We showed that pleiotropy is pervasive and potentially has constrained the evolution of traits. Finally, we recovered variants underlying phenotypic variation at adaptive traits. Because elevation mimics climate change through space, these variants may be relevant for future maize breeding. Author summaryAcross their native range, species encounter a diversity of habitats promoting local adaptation of geographically distributed populations. While local adaptation is widespread, much has yet to be discovered about the conditions of its emergence, the targeted traits, their molecular determinants and the underlying ecological drivers. Here we employed a reverse ecology approach, combining phenotypes and genotypes, to mine the determinants of local adaptation of teosinte populations distributed along two steep altitudinal gradients in Mexico. Evaluation of 11 populations in two common gardens located at mid-elevation pointed to the set-up of an altitudinal syndrome, in spite of gene flow. We scanned genomes to identify loci with allele frequencies shifts along elevation. Interestingly, variation at these loci was commonly associated to variation of phenotypes. Because elevation mimics climate change through space, these variants may be relevant for future maize breeding.

evolutionary biology↗