The genome of the simultaneously hermaphroditic snail Lymnaea stagnalis reveals an evolutionary expansion of FMRFamide-like receptors

Type Article
Acceptance Date 2024-02-12 IN PRESS
Language English
Author(s) Koene Joris M.1, Jackson Daniel J.2, Nakadera Yumi1, Cerveau Nicolas2, Madoui Mohammed-Amin3, Noel Benjamin4, Jamilloux Véronique5, Poulain Julie4, Labadie Karine6, Silva Corinne Da4, Davison Angus7, Feng Zhong-Ping8, Adema Coen M.9, Klopp Christophe10, Aury Jean-Marc4, Wincker Patrick4, Coutellec Marie-Agnès11
Affiliation(s) 1 : Amsterdam Institute for Life and Environment (A-LIFE), Vrije Universiteit, the netherlands
2 : Georg-August University of Göttingen, germany
3 : SEPIA, Institut François Jacob, Université Paris Saclay, france
4 : Génomique Métabolique, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, france
5 : PROSE, INRAE, Paris-Saclay University, france
6 : Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, france
7 : University of Nottingham, uk
8 : King's College, university of toronto, canada
9 : University of New Mexico, usa
10 : INRAE, Applied Mathematics and Informatics of Toulouse, MIAT UR875, france
11 : DECOD (Ecosystem Dynamics and Sustainability), INRAE, L’Institut Agro, france
Source Under Review at Scientific Reports (Research Square Platform LLC) In Press
DOI 10.21203/rs.3.rs-3948809/v1
Note This is a preprint ; it has not been peer reviewed by a journal
Keyword(s) Molluscan genome, nuclear receptors, GPCRs, gene expansion, simultaneous hermaphroditism
Abstract

The great pond snail Lymnaea stagnalis has served as a model organism for over a century in diverse disciplines such as neurophysiology, evolution, ecotoxicology and developmental biology. To support both established uses and newly emerging research interests we have performed whole genome sequencing (~ 176 x depth), assembly and annotation of a single individual derived from an inbred line. These efforts resulted in a final assembly of 943 Mb (L50 = 257; N50 = 957,215) with a total of 22,499 predicted gene models. As a first step towards understanding the hermaphroditic reproductive biology of L. stagnalis, we identified molecular receptors, specifically nuclear receptors (including newly discovered 2xDNA binding domain-NRs), G protein-coupled receptors, and receptor tyrosine kinases, that may be involved in the cellular specification and maintenance of simultaneously active male and female reproductive systems. A phylogenetic analysis of one particular family of GPCRs (Rhodopsin neuropeptide FMRFamide-receptor-like genes) shows a remarkable expansion that coincides with the occurrence of simultaneous hermaphroditism in the Euthyneura gastropods. As some GPCRs and NRs also showed qualitative differences in expression in female (albumen gland) and male (prostate gland) organs, it is possible that separate regulation of male and female reproductive processes may in part have been enabled by an increased abundance of receptors in the transition from a separate-sexed state to a hermaphroditic condition. These findings will support efforts to pair receptors with their activating ligands, and more generally stimulate deeper insight into the mechanisms that underlie the modes of action of compounds involved in neuroendocrine regulation of reproduction, induced toxicity, and development in L. stagnalis, and molluscs in general.

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Koene Joris M., Jackson Daniel J., Nakadera Yumi, Cerveau Nicolas, Madoui Mohammed-Amin, Noel Benjamin, Jamilloux Véronique, Poulain Julie, Labadie Karine, Silva Corinne Da, Davison Angus, Feng Zhong-Ping, Adema Coen M., Klopp Christophe, Aury Jean-Marc, Wincker Patrick, Coutellec Marie-Agnès. The genome of the simultaneously hermaphroditic snail Lymnaea stagnalis reveals an evolutionary expansion of FMRFamide-like receptors. Under Review at Scientific Reports IN PRESS. Publisher's official version : https://doi.org/10.21203/rs.3.rs-3948809/v1 , Open Access version : https://archimer.ifremer.fr/doc/00879/99045/