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Emergence of novel phenotypes in co-evolving biological systems: allelic diversification and dominance at the Self-incompatibility locus in Arabidopsis.

Periodic Reporting for period 3 - NOVEL (Emergence of novel phenotypes in co-evolving biological systems: allelic diversification and dominance at the Self-incompatibility locus in Arabidopsis.)

Reporting period: 2018-10-01 to 2020-03-31

• What is the problem/issue being addressed?
For most biological systems, establishing the link between genotype and phenotype and between phenotype and fitness is a challenge task. In this project, we focus on the sporophytic self-incompatibility system in outcrossing Arabidopsis species, a model biological system in which two distinct co-evolutionary processes are becoming well-understood: 1) between the male and female reproductive proteins allowing self-pollen recognition and rejection and 2) between small non-coding RNAs and their target sites that jointly control the dominance/recessivity interactions between self-incompatibility alleles. By studying these two model systems, we aim to catch the emergence of functional and regulatory novelty in flagrante delicto.

• Why is it important for society?
This project will improve basic knowledge by developping an integrated understanding of not only the proximal causes of phenotypic variation (at the mechanistic level) but also of the ultimate causes (in terms of how natural selection is acting on those variations). This is important in order to improve the predictive power of evolutionary biology, clarifying the molecular constraints on the evolutionary process. At the applied level, the biological system studied –self-incompatibility- is an essential feature of plant mating systems, whose manipulation could lead to improvement of crop breeding procedures.

• What are the overall objectives?
We take a multidisciplinary approach combining theoretical and empirical population genetics, evolutionary genomics and ancestral protein resurrection. Our combination of various powerful approaches in a tractable model system should provide insight on diversification, a poorly understood but fundamental evolutionary process that is taking place at all levels of organization.
We have started both work packages in parallel. Our main results include :
• We have shown that European populations of the self-compatible plant Arabidopsis thaliana has retained only three relict S-alleles, with frequent recombination events among them (Tsuchimatsu et al. MBE 2017).
• We have contributed to a large-scale study of genomic polymorphism in the alloetraploid plant A. suecica, showing that the molecular determinants of dominance/recessivity interactions apparently remain functional (Novikova et al. MBE 2017).
• We have used theoretical models to determine the extent to which stability of self-incompatibility is affected by population subdivision.
• We have constructed and analysed BAC libraries to study haplotype structure of the genomic region flanking the S-locus in natural A. halleri populations
• We have initiated a study to directly follow allelic diversification along the allelic phylogeny
• We have made progress on the understanding of the silencing mechanism controlling dominance/recessivity interactions.
Our ambition is to address consequential evolutionary questions on plant sexual reproduction by integrating approaches ranging from plant molecular biology (to functionally characterize the genetic elements involved) to mathematical modeling to predict the action of natural selection on the variants observed in natural populations. At this early step of the project, we have been able to reach this goal on several tasks of the project. Although most of these tasks are still in progress, we are already understanding better how new self-incompatibility can be formed, both from a molecular perspective and from a theoretical perspective. We are also understanding better the way dominance/recessivity interactions are controlled at the molecular level.