The mechanisms by which flowering plants choose their mating partners have interested researchers for a long time Recent findings on the molecular mechanisms of non-self-recognition in some plant species have provided new insights into self-incompatibility (SI), the trait used by a wide range of plant species to avoid self-fertilization and promote outcrossing In this Review, we compare the known SI systems, which can be largely classified into non-self- or self-recognition systems with respect to their molecular mechanisms, their evolutionary histories and their modes of evolution We review previous controversies on haplotype evolution in the gametophytic SI system of Solanaceae species in light of a recently elucidated non-self-recognition model In non-self-recognition SI systems, the transition from self-compatibility (SC) to SI may be more common than previously thought Reversible transition between SI and SC in plants may have contributed to their adaptation to diverse and fluctuating environments

Non-self- and self-recognition models in plant self-incompatibility

Selfing has evolved in animals, fungi, and plants, and since Darwin's pioneering study, it is considered one of the most frequent evolutionary trends in flowering plants. Generally, the evolution of selfing is characterized by a loss of self-incompatibility, the selfing syndrome, and changes in genome-wide polymorphism patterns. Recent interdisciplinary studies involving molecular functional experiments, genome-wide data, experimental evolution, and evolutionary ecology using Arabidopsis thaliana, Caenorhabditis elegans, and other species show that the evolution of selfing is not merely a degradation of outcrossing traits but a model for studying the recurrent patterns underlying adaptive molecular evolution. For example, in wild Arabidopsis relatives, self-compatibility evolved from mutations in the male specificity gene, S-LOCUS CYSTEINE-RICH PROTEIN/S-LOCUS PROTEIN 11 (SCR/SP11), rather than the female specificity gene, S-LOCUS RECEPTOR KINASE (SRK), supporting the theoretical prediction of sexual asym...

Evolution of Selfing: Recurrent Patterns in Molecular Adaptation

Balancing selection describes any form of natural selection, which results in the persistence of multiple variants of a trait at intermediate frequencies within populations. By offering up a snapshot of multiple co-occurring functional variants and their interactions, systems under balancing selection can reveal the evolutionary mechanisms favouring the emergence and persistence of adaptive variation in natural populations. We here focus on the mechanisms by which several functional variants for a given trait can arise, a process typically requiring multiple epistatic mutations. We highlight how balancing selection can favour specific features in the genetic architecture and review the evolutionary and molecular mechanisms shaping this architecture. First, balancing selection affects the number of loci underlying differentiated traits and their respective effects. Control by one or few loci favours the persistence of differentiated functional variants by limiting intergenic recombination, or its impact, and may sometimes lead to the evolution of supergenes. Chromosomal rearrangements, particularly inversions, preventing adaptive combinations from being dissociated are increasingly being noted as features of such systems. Similarly, due to the frequency of heterozygotes maintained by balancing selection, dominance may be a key property of adaptive variants. High heterozygosity and limited recombination also influence associated genetic load, as linked recessive deleterious mutations may be sheltered. The capture of deleterious elements in a locus under balancing selection may reinforce polymorphism by further promoting heterozygotes. Finally, according to recent genomewide scans, balanced polymorphism might be more pervasive than generally thought. We stress the need for both functional and ecological studies to characterize the evolutionary mechanisms operating in these systems.

Genetic architecture and balancing selection: the life and death of differentiated variants.

The self-incompatible species Arabidopsis halleri is a close relative of the self-compatible model plant Arabidopsis thaliana. The broad European and Asian distribution and heavy metal hyperaccumulation ability make A. halleri a useful model for ecological genomics studies. We used long-insert mate-pair libraries to improve the genome assembly of the A. halleri ssp. gemmifera Tada mine genotype (W302) collected from a site with high contamination by heavy metals in Japan. After five rounds of forced selfing, heterozygosity was reduced to 0.04%, which facilitated subsequent genome assembly. Our assembly now covers 196 Mb or 78% of the estimated genome size and achieved scaffold N50 length of 712 kb. To validate assembly and annotation, we used synteny of A. halleri Tada mine with a previously published high-quality reference assembly of a closely related species, Arabidopsis lyrata. Further validation of the assembly quality comes from synteny and phylogenetic analysis of the HEAVY METAL ATPASE4 (HMA4) and METAL TOLERANCE PROTEIN1 (MTP1) regions using published sequences from European A. halleri for comparison. Three tandemly duplicated copies of HMA4, key gene involved in cadmium and zinc hyperaccumulation, were assembled on a single scaffold. The assembly will enhance the genomewide studies of A. halleri as well as the allopolyploid Arabidopsis kamchatica derived from A. lyrata and A. halleri.

https://www.zora.uzh.ch/id/eprint/126774/1/Briskine_et_al-2016-Molecular_Ecology_Resources.pdf

Genome assembly and annotation of Arabidopsis halleri, a model for heavy metal hyperaccumulation and evolutionary ecology

Polyploidy is an example of instantaneous speciation when it involves the formation of a new cytotype that is incompatible with the parental species. Because new polyploid individuals are likely to be rare, establishment of a new species is unlikely unless polyploids are able to reproduce through self-fertilization (selfing), or asexually. Conversely, selfing (or asexuality) makes it possible for polyploid species to originate from a single individual-a bona fide speciation event. The extent to which this happens is not known. Here, we consider the origin of Arabidopsis suecica, a selfing allopolyploid between Arabidopsis thaliana and Arabidopsis arenosa, which has hitherto been considered to be an example of a unique origin. Based on whole-genome re-sequencing of 15 natural A. suecica accessions, we identify ubiquitous shared polymorphism with the parental species, and hence conclusively reject a unique origin in favor of multiple founding individuals. We further estimate that the species originated after the last glacial maximum in Eastern Europe or central Eurasia (rather than Sweden, as the name might suggest). Finally, annotation of the self-incompatibility loci in A. suecica revealed that both loci carry non-functional alleles. The locus inherited from the selfing A. thaliana is fixed for an ancestral non-functional allele, whereas the locus inherited from the outcrossing A. arenosa is fixed for a novel loss-of-function allele. Furthermore, the allele inherited from A. thaliana is predicted to transcriptionally silence the allele inherited from A. arenosa, suggesting that loss of self-incompatibility may have been instantaneous.

https://hal.archives-ouvertes.fr/hal-01605859/document

Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica

The prevention of fertilization through self-pollination (or pollination by a close relative) in the Brassicaceae plant family is determined by the genotype of the plant at the self-incompatibility locus (S locus). The many alleles at this locus exhibit a dominance hierarchy that determines which of the two allelic specificities of a heterozygous genotype is expressed at the phenotypic level. Here, we uncover the evolution of how at least 17 small RNA (sRNA)-producing loci and their multiple target sites collectively control the dominance hierarchy among alleles within the gene controlling the pollen S-locus phenotype in a self-incompatible Arabidopsis species. Selection has created a dynamic repertoire of sRNA-target interactions by jointly acting on sRNA genes and their target sites, which has resulted in a complex system of regulation among alleles.

https://science.sciencemag.org/content/sci/346/6214/1200.full.pdf

Marion Soucaze

Papers

Dominance hierarchy arising from the evolution of a complex small RNA regulatory network.