The evolution and regulation of major transitions in sexual systems: new insights from the brown algae

Project Information

TETHYS

Grant agreement ID: 864038

DOI

10.3030/864038

Project closed

EC signature date 20 December 2019

Start date 1 January 2021

End date 31 December 2025

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 999 420,00

EU contribution

€ 1 999 420,00

Coordinated by

MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN EV
Germany

Periodic Reporting for period 3 - TETHYS (The evolution and regulation of major transitions in sexual systems: new insights from the brown algae)

Reporting period: 2024-01-01 to 2025-06-30

Summary of the context and overall objectives of the project

The overarching goal of the Tethys project is to decipher the mechanisms and ultimate forces shaping major transitions between sexual systems during the evolution of the brown algae. First, we are exploiting genomic resources and the amenability of brown algae to genetic approaches to uncover the genetic causes, the mechanisms and evolutionary forces shaping transitions between sexual systems across this group. We focus on transitions between separate and combined sexes during the haploid (dioicy to monoicy) and diploid phases (monoecy and dioecy) but also on a major evolutionary transition from haploid to diploid sex determination. We expect to reveal the causal genes and downstream effectors involved in the diversity of sexual systems and to elucidate the forces driving switches between systems. Second, we investigate the regulation and evolution of genes involved in sexual reproduction in the context of sexual system transitions, by delineating a comprehensive transcriptional and chromatin state roadmap for sexual development across key brown algal species. These analyses is uncovering the evolution of the genetic programs involved in sexual system transitions and revealing their higher-order regulation via chromatin remodelling. Third, we examine patterns of correlated evolution between sexual, morphological and genomic traits and incorporate ecological information in a phylogenetic context, in order to link ecological factors with reproductive transitions and evaluate the consequences of shifts in sexual systems on genome structure and species diversification. Collectively, our multilevel analyses is revealing the fundamental forces shaping major transitions in sexual systems with wide relevance to all eukaryotes, but also providing insights into the biology of an important but virtually unexplored eukaryotic supergroup.

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

1. We have unveiled the nature, evolution and degree of convergence of the molecular changes that accompany the breakdown of dioicy, i.e. the transition from separate sexes to hermaphroditism. Cossard et al Nature Ecol. Evol. 2022
2. By exploiting inbred pedigrees of the brown algae Ectocarpus and Scytosiphon, we accessed for the first time to the spontaneous mutation rate of representative organisms of a complex multicellular eukaryotic lineage outside animals and plants, and revealed the impact of life cycle on mutation rate. Krasovec et al MBE 2023
3. We explored isogenic male and female lines of the model brown alga Ectocarpus and employed sex-specific transcriptomic and ChIP-seq datasets to disclose the chromatin dynamics underlying sexual differentiation. Our findings offered new, comparative insights into the interactions between chromatin configurations and gene expression patterns in males versus females, with wide implications to animal and plant systems. Gueno et al. 2022
4. We provide the first illustration of how male- and female-specific developmental programs in a haploid sex determination system may be uncoupled from sex chromosome identity. We reveal new and key aspects of the evolution of sex-specific and sex-biased gene expression patterns in the third most complex multicellular eukaryotic lineage3, increasing our knowledge on evolution of sexual dimorphism in the context of the Tree of Life. (Muller et al New Phyt 2022)
5. We have produced an Atlas of gene expression for 22 species across the phylogeny of the brown algae, and covering 6-15 stages of development during their life cycle. This Seaweed Expression Atlas is being used to understand the emergence and evolution of multicellular development and sexual differentiation. We are building a database that will be an open resource for the scientific community.

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)

Tethys is expected to answer long-standing key evolutionary questions about the diversity and turnover of sex determining systems in eukaryotes, with significant potential to make discoveries concerning the genetic and epigenetic mechanisms involved in transitions among sex determination mechanisms with relevance to all eukaryotes. Importantly, our project offesr a broader taxonomic view on the evolution of sexual systems, exploring avenues away from the classical plant-animal dichotomy, and allowing access to the universality, or uniqueness, of the mechanisms driving fundamental biological processes in the context of the tree of life.

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