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Vekemans, X.

Publications and source records attributed to Vekemans, X..

At least 19 recordsLinked to original sources

Genotyping the self-incompatibility locus of wild and cultivated Brassica using NGS technologies: application to the evaluation of mate limitation in the endangered species Brassica insularis

O_LISelf-incompatibility can limit the availability of compatible mates in small and isolated populations, eventually reducing average seed set to the point that the long-term persistence of the populations can be impaired. This phenomenon, named the S-Allee effect, is caused by the loss of alleles (S-alleles) at the self-incompatibility locus (S-locus) due to the intense genetic drift experienced by small populations. Quantifying the diversity of S-alleles is therefore of direct interest for biological conservation, but efficient genotyping methods have been lacking so far because of technical challenges associated with the typically extreme levels of polymorphism and complex genomic structure of the S-locus. C_LIO_LIWe used two alternative approaches to genotype the S-locus using NGS sequencing technologies in four natural populations of the endangered Brassica insularis in Corsica. First, we used an NGS amplicon-sequencing approach using generalist primers for each of the two classes of Brassica S-alleles. Second, we obtained whole genome shotgun short-read resequencing data and analyzed them with a recently developed bioinformatic pipeline dedicated to hypervariable loci, which we successfully validated on a public dataset comprising 119 cultivated accessions of B. oleracea. C_LIO_LIBy combining the two approaches in natural populations of B. insularis we identified 31 distinct S-alleles and obtained fully resolved S-locus genotypes for 319 out of 326 sampled individuals. The number of S-alleles varied from four in the smallest population to 18 in the largest one. As a result, the smallest population exhibited very low proportions of compatible individuals, potentially threatening its persistence. We conclude that introducing individuals carrying S-alleles currently absent from the population could help rescue fertility. C_LI

evolutionary biology↗

Breakdown of sporophytic self-incompatibility: Diploids versus tetraploids

Many angiosperm species possess self-incompatibility (SI) systems that prevent self-fertilization. Because empirical studies often report higher selfing rates in tetraploids than in diploids, we investigate whether sporophytic self-incompatibility (SSI) is more likely to break down after the introduction of a self-compatible (SC) allele in tetraploid populations. To address this question, we use analytical models and individual-based simulations to compare diploid and tetraploid populations under two main scenarios: (1) all SI alleles are codominant, and (2) SI alleles are structured into dominance classes. Overall, our results indicate that SSI is more difficult to maintain in tetraploids than in diploids, with dominance relationships playing a key role in the invasion success of an SC allele. When SI alleles are organized into dominance classes, increasing the dominance of the SC allele generally favors SSI breakdown in tetraploids, while diploids show weaker sensitivity to dominance, with SSI maintained across all dominance scenarios for the SC allele under sufficiently high inbreeding depression. However, when the SC allele is dominant over all SI alleles, SSI is more readily maintained in both the codominant and dominance-class models.

plant biology↗

Autopolyploid establishment under gametophytic self-incompatibility: the impact of self-fertilization and pollen limitation

Polyploidy is widespread in plants, yet the establishment of neo-polyploids is limited by minority cytotype exclusion (MCE). As polyploidy has been associated with higher selfing rates in empirical studies, a shift from self-incompatibility (SI) to self-compatibility (SC) may help overcome MCE, particularly under ga-metophytic SI (GSI) with non-self-recognition where an automatic shift to SC is associated with polyploidy. We investigated theoretically the joint evolution of polyploidy and self-compatibility and its impact on tetraploid establishment in initially diploid populations with GSI under different pollen limitation scenar-ios, and with fixed or variable selfing rates for polyploids. It is shown that, for high pollen limitation scenarios, autotetraploids can invade an initially diploid population only when the selfing rates are high. Under low pollen limitation, the conditions for tetraploid invasion are less restrictive (selfing rates above 0.3). These results apply to scenarios with either fixed or variable selfing rates in polyploids, but in the latter, high mutation rates of the selfing rate are needed for polyploidy to invade. These results suggest that tetraploid establishment is possible through the evolution of selfing, without introducing a non-functional S-allele. However, the conditions strongly depend on the degree of pollen limitation.

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↗

Autopolyploidy exacerbates dominance masking under negative frequency-dependent selection: evidence from sporophytic self-incompatibility in Arabidopsis arenosa and A. lyrata

Polyploidy is a widespread phenomenon in flowering plants, with up to 30% of extant species being recent polyploids. Whether and how polyploidy modulates the action of natural selection remains debated, and the particular case of balancing selection has been poorly explored. This study investigates the impact of autopolyploidy on sporophytic self-incompatibility in plants, a striking example of a genetic system evolving under a special form of balancing selection (strong negative frequency-dependent selection). Numerical simulations reveal that under strict codominance, the number of S-alleles maintained in tetraploid populations is expected to double as compared to diploid populations. However, under a model with strict hierarchical dominance among alleles, the number of S-alleles increases only slightly, but gene diversity and observed heterozygosity are substantially lower in tetraploids as compared to diploids, due to enhanced dominance masking effects. Empirical data on Arabidopsis arenosa and A. lyrata confirm the latter predictions, showing similar levels of allelic diversity but dramatically lower observed and expected heterozygosity at the self-incompatibility locus in tetraploids compared to diploids. The study highlights the significant impact of autopolyploidy on patterns of diversity at the self-incompatibility locus, emphasizing the increased dominance effect in tetraploids. The results also allow us to reject a scenario of strong founder effects associated with evolution of the polyploid lineages.

evolutionary biology↗

Modifiers of genetic dominance at the Arabidopsis self-incompatibility locus retain proto-miRNA features and act through non-canonical gene silencing pathways

Self-incompatibility in flowering plants is a common mechanism that prevents self-fertilization and promotes outcrossing. In Brassicaceae, the self-incompatibility locus is highly diverse, with many alleles arranged in a complex dominance hierarchy and exhibiting monoallelic expression in heterozygote individuals. Monoallelic expression of the pollen self-incompatibility gene is achieved through the action of sRNA precursors that resemble miRNAs, although the underlying molecular mechanisms remain elusive. Here, we engineered Arabidopsis thaliana lines expressing components of the Arabidopsis halleri self-incompatibility system, and used a reverse genetics approach to pinpoint the pathways underlying the function of these sRNA precursors. We showed that they trigger a robust decrease in transcript abundance of the recessive self-incompatibility genes, but not through the canonical transcriptional or post-transcriptional gene silencing pathways. Furthermore, we observed that single sRNA precursors are typically processed into hundreds of sRNA molecules with a variety of sizes, abundance levels and ARGONAUTE loading preferences. Our results suggest that these seemingly arbitrary processing characteristics are essential for establishing the self-incompatibility dominance hierarchy, as they enable a single sRNA precursor from a dominant allele to effectively repress multiple recessive alleles, thus providing a unique example of how small RNAs mediate gene silencing within a highly complex regulatory network. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=80 SRC="FIGDIR/small/591913v3_ufig1.gif" ALT="Figure 1"> View larger version (24K): org.highwire.dtl.DTLVardef@b32c02org.highwire.dtl.DTLVardef@10e65d3org.highwire.dtl.DTLVardef@3f14b3org.highwire.dtl.DTLVardef@1682d57_HPS_FORMAT_FIGEXP M_FIG C_FIG

plant biology↗

The diallelic self-incompatibility system in Oleaceae is controlled by a hemizygous genomic region expressing a gibberellin pathway gene

Sexual reproduction in flowering plants is commonly controlled by self-incompatibility (SI) systems that are either homomorphic (and typically governed by large numbers of distinct allelic specificities), or heteromorphic (and then typically governed by only two allelic specificities). The SI system of the Oleaceae family is a striking exception to this rule and represents an evolutionary conundrum, with the long-term maintenance of only two allelic specificities, but often in the complete absence of morphological differentiation between them. To elucidate the genomic architecture and molecular bases of this highly unusual SI system, we obtained chromosome-scale genome assemblies of Phillyrea angustifolia individuals belonging to the two SI specificities and connected them to a genetic map. Comparison of the S-locus region revealed a segregating 543-kb indel specific to one of the two specificities, suggesting a hemizygous genetic architecture. Only one of the predicted genes in this indel is conserved with the olive tree Olea europaea, where we also confirmed the existence of a segregating hemizygous indel. We demonstrated full association between presence/absence of this gene and the SI groups phenotypically assessed across six distantly related Oleaceae species. This gene is predicted to be involved in catabolism of the Gibberellic Acid (GA) hormone, and experimental manipulation of GA levels in developing buds modified the male and female SI responses in an S-allele-specific manner. Thus, our results provide a unique example of a reproductive system where a single conserved gibberellin-related gene in a 500-700kb hemizygous indel underlies the long-term maintenance of two groups of reproductive compatibility.

evolutionary biology↗

The genetic architecture of the load linked to dominant and recessive self-incompatibility alleles in Arabidopsis halleri and A. lyrata

The long-term balancing selection acting on mating-types or sex determining genes is expected to lead to the accumulation of deleterious mutations in the tightly linked chromosomal segments that are locally "sheltered" from purifying selection. However, the factors determining the extent of this accumulation are poorly understood. Here, we took advantage of variations in the intensity of balancing selection along a dominance hierarchy formed by alleles at the sporophytic self-incompatibility system of the Brassicaceae to compare the pace at which linked deleterious mutations accumulate among them. We first experimentally measured the phenotypic manifestation of the linked load at three different levels of the dominance hierarchy. We then sequenced and phased polymorphisms in the chromosomal regions linked to 126 distinct copies of S-alleles in two populations of Arabidopsis halleri and three populations of A. lyrata. We find that linkage to the S-locus locally distorts phylogenies over about 10-30kb along the chromosome. The more intense balancing selection on dominant S-alleles results in greater fixation of linked deleterious mutations, while recessive S-alleles accumulate more linked deleterious mutations that are segregating. Hence, the structure rather than the overall magnitude of the linked genetic load differs between dominant and recessive S-alleles. Our results have consequences for the long-term evolution of new S-alleles, the evolution of dominance modifiers between them, and raise the question of why the non-recombining regions of some sex and mating type chromosomes expand over evolutionary times while others, such as that the S-locus of the Brassicaceae, remain restricted to small chromosomal regions.

evolutionary biology↗

Rapid establishment of species barriers in plants compared to animals

Speciation, the process through which new reproductively isolated species emerge from ancestral populations, occurs due to the gradual accumulation of barriers to gene flow within genomes. To date, the notion that interspecific genetic exchange occurs more frequently between plant species than animals species has gained a strong footing in the scientific discourse. By examining the dynamics of gene flow across a continuum of divergence in both kingdoms, we observe the opposite relationship: plants experience less introgression than animals at the same level of genetic divergence, suggesting that species barriers are established more rapidly in plants. This pattern raises questions about which differences in microevolutionary processes between plants and animals influence the dynamics of reproductive isolation establishment at the macroevolutionary scale. One Sentence SummaryGenetic exchange is more frequent between animal species than plants, challenging historical views.

evolutionary biology↗

Dominance between self-incompatibility alleles determines the mating system of Capsella allopolyploids

The shift from outcrossing to self-fertilization is one of the main evolutionary transitions in plants, and has broad effects on evolutionary trajectories. In Brassicaceae, the ability to impede self-fertilization is controlled by two genes, SCR and SRK, tightly linked within the S-locus. A series of small non-coding RNAs also encoded within the S-locus regulates the transcriptional activity of SCR alleles, resulting in a linear dominance hierarchy between them. Brassicaceae allopolyploid species are often self-compatible (SC) even when one of their parents is self-incompatible, but the causes of the loss of self-incompatibility (SI) in polyploid lineages have generally remained elusive. We used a series of synthetic hybrids obtained between self-fertilizing Capsella orientalis and outcrossing C. grandiflora to test whether the breakdown of SI in allopolyploid species, such as C. bursa-pastoris, could be explained by the dominance interactions between S-haplotypes inherited from the parental lineages. After establishing a database of reference S-allele sequences, we used RNA-sequencing data from young inflorescences to measure allele-specific expression of the SCR and SRK genes in diploid and tetraploid synthetic hybrids. We then compared the observed expression of SCR alleles with the predicted dominance relationship between S-haplotypes in pollen and with the seed set from autonomous self-fertilization in the synthetic hybrids. Our results formally establish that upon hybridization, the immediate effect on the mating system depends on the relative dominance between S-alleles inherited from the parental species. They illustrate that a detailed understanding of the genetic architecture of the control of SI is essential to predict the patterns of association between the mating system and changes in ploidy. Lay summaryPolyploidy is the inheritable condition of carrying more than two sets of chromosomes. It can result from within-species genome duplication (auto-polyploidy), or from the merging of sets of chromosomes from different species following hybridization (allo-polyploidy). Because sexual reproduction between individuals of different levels of ploidy is generally not successful, self-fertilization has been considered a key component of the establishment success of polyploid lineages. However, the reasons why the mating system of polyploids may differ from that of their parental species remains mysterious. In plants of the Brassicaceae family, several allopolyploid species arose from hybridization between an outcrossing and a self-fertilizing species, and in most cases the resulting lineages are self-fertilizing. It has been proposed that the mating system of these allopolyploids depends on the dominance relationships between the functional and non-functional self-incompatibility alleles inherited from the parental species. Here, we tested this prediction by characterizing at the transcriptional (RNA-seq) and phenotypic levels (estimation of autonomous seed production) a series of synthetic Capsella diploid and tetraploid hybrids. We found that the predicted dominance relationships matched the observed expression of self-incompatibility alleles, as well as the mating system phenotypes. Hence, the mating system of newly formed Capsella allotetraploids depends on the dominance relationship between self-incompatibility alleles inherited from the parents. Overall, our results improve our understanding of the mechanisms by which changes in ploidy can alter the system of mating over the course of evolution.

evolutionary biology↗

Genome of selfing Siberian Arabidopsis lyrata explains establishment of allopolyploid Arabidopsis kamchatica

A transition to selfing can be beneficial when mating partners are scarce, for example, due to ploidy changes or at species range edges. Here we explain how self-compatibility evolved in diploid Siberian Arabidopsis lyrata, and how it contributed to the establishment of allotetraploid A. kamchatica. First, we provide chromosome-level genome assemblies for two self-fertilizing diploid A. lyrata accessions, one from North America and one from Siberia, including a fully assembled S-locus for the latter. We then propose a sequence of events leading to the loss of self-incompatibility in Siberian A. lyrata, date this independent transition to [~]90 Kya, and infer evolutionary relationships between Siberian and North American A. lyrata, showing an independent transition to selfing in Siberia. Finally, we provide evidence that this selfing Siberian A. lyrata lineage contributed to the formation of the allotetraploid A. kamchatica and propose that the selfing of the latter is mediated by the loss-of-function mutation in a dominant S-allele inherited from A. lyrata.

plant biology↗

Long-term balancing selection and the genetic load linked to the self-incompatibility locus in Arabidopsis halleri and A. lyrata.

Balancing selection is a form of natural selection maintaining diversity at the sites it targets and at linked nucleotide sites. Due to selection favouring heterozygosity, it has the potential to facilitate the accumulation of a "sheltered" load of tightly linked recessive deleterious mutations. However, precisely evaluating the extent of these effects has remained challenging. Taking advantage of plant self-incompatibility as one of the best-understood examples of long-term balancing selection, we provide a highly resolved picture of the genomic extent of balancing selection on the sheltered genetic load. We used targeted genome resequencing to reveal polymorphism of the genomic region flanking the self-incompatibility locus in three sample sets in each of the two closely related plant species Arabidopsis halleri and A. lyrata, and used 100 control regions from throughout the genome to factor out differences in demographic histories and/or sample structure. Nucleotide polymorphism increased strongly around the S-locus in all sample sets, but only over a limited genomic region, as it became indistinguishable from the genomic background beyond the first 25-30kb. Genes in this chromosomal interval exhibited no excess of mutations at 0-fold degenerated sites relative to putatively neutral sites, hence revealing no detectable weakening of the efficacy of purifying selection even for these most tightly linked genes. Overall, our results are consistent with the predictions of a narrow genomic influence of linkage to the S-locus, and clarify how natural selection in one genomic region affects the evolution of the adjacent genomic regions.

genomics↗

Inferring the demographic history of tetraploid species from genomic data

Genomic patterns of diversity and divergence are impacted by certain life history traits, reproductive systems and demographic history. The latter is characterised by fluctuations in population sizes over time, as well as by temporal patterns of introgression. For a given organism, identifying a demographic history that deviates from the standard neutral model allows a better understanding of its evolution, but also helps to reduce the risk of false positives when screening for molecular targets of natural selection. Tetraploid organisms and beyond have demographic histories that are complicated by the mode of polyploidisation, the mode of inheritance and different scenarios of gene flow between subgenomes and diploid parental species. Here we provide guidelines for experimenters wishing to address these issues through a flexible statistical framework: approximate Bayesian computation (ABC). The emphasis is on the general philosophy of the approach to encourage future users to exploit the enormous flexibility of ABC beyond the limitations imposed by generalist data analysis pipelines.

genomics↗

DILS : Demographic Inferences with Linked Selection by using ABC

We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single-population or two-population datasets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: 1) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, 2) the best genomic model to determine whether the effective size Ne and migration rate N.m are heterogeneously distributed along the genome (implying linked selection) and 3) loci in genomic regions most associated with barriers to gene flow. Also available via a web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations, and finally apply the method to published data on a divergence continuum composed by 28 pairs of Mytilus mussel populations/species.

evolutionary biology↗

A New Tree-Based Methodological Framework to Infer the Evolutionary History of Mesopolyploid Lineages: An Application to the Brassiceae Tribe (Brassicaceae).

Whole genome duplication events are notably widespread in plants and this poses particular challenges for phylogenetic inference in allopolyploid lineages, i.e. lineages that result from the merging of two or more diverged genomes after interspecific hybridization. The nuclear genomes resulting from allopolyploidization contain homologous gene copies from different evolutionary origins called homoeologs, whose orthologs must be sorted out in order to reconstruct the evolutionary history of polyploid clades. In this study, we propose a methodological approach to resolve the phylogeny of allopolyploid clades focusing on mesopolyploid genomes, which experienced some level of genome reshuffling and gene fractionation across their subgenomes. To illustrate our methodological framework we applied it to a clade belonging to the model Brassicaceae plant family, the Brassiceae tribe, that experienced a mesohexaploidy event. The dataset analysed consists of both publically available genomic sequences and new transcriptomic data according to taxa. The present methodology requires a well-annotated reference genome, for which the identification of the parental subgenome fragments has been performed (e.g. Brassica rapa and Brassica oleracea). Focusing on fully retained genes (i.e. genes for which all homoeologous gene copies inherited from the parental lineages are still present in the reference genome), the method constructs multi-labelled gene trees that allow subsequent assignment of each gene copy to its diploid parental lineage. Once the orthologous copies are identified, genes from the same parental origin are concatenated and tree-building methods are used to reconstruct the species tree. This method allows resolving the phylogenetic relationships (i) among extant species within a mesopolyploid clade, (ii) among the parental lineages of a mesopolyploid lineage, and (iii) between the parental lineages and closely related extant species. We report here the first well-resolved nuclear-based phylogeny of the Brassiceae tribe.

evolutionary biology↗

High throughput, high fidelity genotyping and de novo discovery of allelic variants at the self-incompatibility locus in natural populations of Brassicaceae from short read sequencing data

Plant self-incompatibility (SI) is a genetic system that prevents selfing and enforces outcrossing. Because of strong balancing selection, the genes encoding SI are predicted to maintain extraordinary high levels of polymorphism, both in terms of the number of S-alleles that segregate in SI species and in terms of nucleotide sequence divergence among distinct S-allelic lines. However, because of these two combined features, documenting polymorphism of these genes also presents important methodological challenges that have so far largely prevented the comprehensive analysis of complete allelic series in natural populations, and also precluded the obtention of complete genic sequences for many S-alleles. Here, we present a novel methodological approach based on a computationally optimized comparison of short Illumina sequencing reads from genomic DNA to a database of known nucleotide sequences of the extracellular domain of SRK (eSRK). By examining mapping patterns along the reference sequences, we obtain highly reliable predictions of S-genotypes from individuals collected in natural populations of Arabidopsis halleri. Furthermore, using a de novo assembly approach of the filtered short reads, we obtain full length sequences of eSRK even when the initial sequence in the database was only partial, and we discover new SRK alleles that were not initially present in the database. When including those new alleles in the reference database, we were able to resolve the complete diploid SI genotypes of all individuals. Beyond the specific case of Brassicaceae S-alleles, our approach can be readily applied to other polymorphic loci, given reference allelic sequences are available.

evolutionary biology↗

Asymmetrical diversification of the receptor-ligand interaction controlling self-incompatibility in Arabidopsis

How two-components genetic systems accumulate evolutionary novelty and become diversified in the course of evolution is a fundamental problem in evolutionary systems biology. In the Brassicaceae, self-incompatibility (SI) is a spectacular example of a diversified allelic series in which numerous highly diverged receptor-ligand combinations are segregating in natural populations. However, the evolutionary mechanisms by which new SI specificities arise in the first place have remained elusive. Using in planta ancestral protein resurrection, we demonstrate that two allelic variants currently segregating as distinct receptor-ligand combinations diverged through an asymmetrical process whereby one variant has retained the same recognition specificity as the (now extinct) ancestor, while the other has functionally diverged and now represents a novel specificity no longer recognized by the ancestor. Examination of the structural determinants of the shift in binding specificity suggests that allosteric changes may be an important source of evolutionary novelty in this highly diversified receptor-ligand system.

evolutionary biology↗

Maintenance of adaptive dynamics in a bottlenecked range-edge population that retained outcrossing

During range expansion, edge populations are expected to face increased genetic drift, which in turn can alter and potentially compromise adaptive dynamics, preventing the removal of deleterious mutations and slowing down adaptation. Here, we contrast populations of the European sub-species Arabidopsis lyrata ssp petraea, which expanded its Northern range after the last glaciation. We document a sharp decline in effective population size in the range-edge population and observe that non-synonymous variants segregate at higher frequencies. We detect a 4.9% excess of derived non-synonymous variants per individual in the range-edge population, suggesting an increase of the genomic burden of deleterious mutations. Inference of the fitness effects of mutations and modeling of allele frequencies under the explicit demographic history of each population predicts a depletion of rare deleterious variants in the range-edge population, but an enrichment for fixed ones, consistent with the bottleneck effect. However, the demographic history of the range-edge population predicts a small net decrease in per-individual fitness. Consistent with this prediction, the range-edge population is not impaired in its growth and survival measured in a common garden experiment. We further observe that the allelic diversity at the self-incompatibility locus, which ensures strict outcrossing and evolves under negative frequency-dependent selection, has remained unchanged. Genomic footprints indicative of selective sweeps are broader in the Northern population but not less frequent. We conclude that the outcrossing species A. lyrata ssp petraea shows a strong resilience to the effect of range expansion.

evolutionary biology↗