Search bioRxiv⌕ Search

Biology subjects

Poux, C.

Publications and source records attributed to Poux, C..

5 recordsLinked to original sources

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↗

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↗

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↗

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↗

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↗