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SEXSEA Report Summary

Project ID: 638240
Funded under: H2020-EU.1.1.

Periodic Reporting for period 1 - SEXSEA (Origin and evolution of the sexes and reproductive systems: novel insights from a distant eukaryotic lineage)

Reporting period: 2015-06-01 to 2016-11-30

Summary of the context and overall objectives of the project

Sexual reproduction is an extraordinarily widespread phenomenon that assures the production of new genetic combinations in nearly all eukaryotic lineages. Although the core mechanisms of sexual reproduction (meiosis and syngamy) are highly conserved, the control mechanisms that determine whether an individual is male or female are remarkably labile across eukaryotes. In genetically controlled sexual systems, gender is determined by sex chromosomes, which have emerged independently and repeatedly during evolution. Sex chromosomes have been studied in only a handful of classical model organism, and empirical knowledge on the origin and evolution of the sexes is still surprisingly incomplete. The goal of our project is to exploit the remarkable richness of sexual characteristics of the brown algae to gain novel insights into the functional and evolutionary interactions between the sex chromosomes and key eukaryotic reproductive and life cycle features. First, we are using the model brown alga Ectocarpus to reveal the fundamental genetic mechanisms by which sex chromosomes control reproductive and life cycle traits of broad importance to all eukaryotes, including sex determination and asexual reproduction through parthenogenesis but also the control of gamete size and the regulation of developmental switches during the life cycle. Secondly, we are employing a combination of experimental and computational approaches on selected brown algal species exhibiting a range of reproductive and life cycle features to understand the long term evolutionary consequences of the variations in these traits to the structure of their sex chromosomes, in a phylogenetic context. These analyses will not only reveal fundamental forces that shape sex chromosome evolution in the scope of the tree of life, but will also uncover the mechanisms underlying important evolutionary transitions between major reproductive and life cycle modes and shed new light on the origin and evolution of the sexes.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

We investigated the evolution of the model brown algal Ectocarpus sex chromosomes using a combination of genomic and molecular evolution approaches. We compared gene organisation, quantified levels of divergence, distribution of transposable elements, etc between the two haplotypes of the sex determining region, and compared the Ectocarpus sex chromosomes with those of distantly related brown algal species gain knowledge on the origin and evolution of sexes in this group of organisms. These analyses provided information about the age of the sex chromosomes in brown algae but also allowed us to test existing hypotheses about the evolutionary trajectories of sex determining regions in organisms that express sex during the haploid phase of their life cycle (haploid sex determination systems). Importantly, our analysis has also provided unprecedented information about the recombining region of the sex chromosome (pseudo autosomal region). We have sequenced and analysed the genomes of seven brown alga species belonging to different clades to study gene conservation in the sex chromosome. A core set of sex-linked genes were conserved across all the brown algal species investigated, but we also identified modifications of the sex-determining regions of the sex chromosome that occurred in a lineage-specific fashion. These modifications involved gene loss, gene gain from the pseudo-autosomal regions and from autosomes and relocation of genes from the SDR to autosomes. We have identified a candidate master male determining gene that has been stably male-linked across 100 million years of the brown algal evolutionary history. We are currently further validating this gene and using molecular approaches to understand how this master sex determining gene is triggering sex determination and sexual differentiation.
We have used transcriptomic approaches to investigate the origin and evolution of sexual dimorphism by taking advantage of the genomic and transcriptomic datasets from brown algal presenting contrasting levels of male-female differentiation. We are generating mutants affected in their gamete size in order to gain knowledge on the link between phenotypic and genotypic sexual dimorphism. One interesting sexual dimorphic trait is the parthenogenetic capacity of gametes, and we have used QTL and Shoremap approaches to identify the genomic regions involved in this trait, and to understand how the sex determining regions and the parthenogenesis locus interact.
We have prepared segregating populations for several different brown algae and started the construction of genetic maps that will be used for higher scale genome assembly and for comparative genomic analysis.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

- Full characterisation of the sex chromosomes of a model organism from an important multicellular eukaryotic lineage
- Identification of a candidate master sex determination gene
- Identification of the evolutionary forces affecting the evolution of haploid sex chromosomes
- Validation and substantial expansion of existing models for the evolution of the sexes
- Identification of sex-markers for algae with important economic interest (kelps), which will not only facilitate seaweed breeding programs but also represent useful tools for population and demography studies

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