EVOBOOSTER - Impact of transposable elements on gene regulatory networks: application to fast-evolving biological pathways in fish
General Genetics and Functional Genome Biology
Final Report Abstract
In teleost fish, as in other organisms, sexual reproduction and sexual gene regulatory networks are highly variable. In gonochoristic species, sex is determined either environmentally or genetically and can involve different genes depending on the species investigated. Sexual development and maintenance appear also variable in this clade. Another fast evolving trait is pigmentation, where fish also show an astonishing diversity in some groups. To understand the origin of this diversity, we studied the possible impact of transposable elements (TEs) on the fast evolution of gene regulatory networks related to sex and pigmentation in fish. Transposable elements are genomic endogenous DNA sequences able to move or copy themselves in genomes. Even if they are often deleterious for their host, TEs can also carry regulatory sequences, such as transcription factor binding sites, and spread them in genomes. Their diversity in fish genomes constitutes a source of readyto-use regulatory sequences potentially involved in the fast evolution of sex-biased gene regulatory networks. We have shown for the first time that genes and TEs with a similar sex-biased expression are not randomly distributed in the genome but tend to colocalize within clusters in the same genomic regions, a functional organization implying common regulations and reciprocal regulatory interactions. Accordingly, close genes and TEs tend to have similar expression patterns in gonads. We have also identified specific families of TEs frequently associated with sex-biased genes. A candidate family has been more particularly studied, which carries binding sites for transcription factors known to be involved in sexual development. In some cases, absence of the TE insertion from the gene in some Oryzias species was associated with absence of sex-biased expression. Crispr-Cas9 deletion of insertions associated with gene sex biased-expression has been initiated to functionally demonstrate the role of the TE in sex-biased expression. In the pigment cell lineage we found an increased expression of full length TE in highly malignant lesions indicating their activity. We hypothesize that active TEs may contribute to genomic instability of melanoma. This work brings new insights into the possible role of transposable elements in the fast evolution of gene regulatory networks and genome integrity and paves the way for future functional studies.
Publications
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(2019) Sex and the TEs: transposable elements in sexual development and function in animals. Mobile DNA 10:42
Corentin Dechaud, Jean-Nicolas Volff, Manfred Schartl, Magali Naville
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(2021) Clustering of sex-biased genes and transposable elements in the genome of the medaka fish O. latipes. Genome Biology and Evolution 13:evab230
Corentin Dechaud, Sho Miyake, Anabel Martinez-Bengochea, Manfred Schartl, Jean- Nicolas Volff, Magali Naville
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(2021) Differential expression of transposable elements in the medaka melanoma model. PLoS One 16:e0251713
Frederik Helmprobst, Susanne Kneitz, Barbara Klotz, Magali Naville, Corentin Dechaud, Jean- Nicolas Volff, Manfred Schartl
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(2021) Giant lungfish genome elucidates the conquest of land by vertebrates. Nature 590:284-289
Axel Meyer, Siegfried Schloissnig, Paolo Franchini, Kang Du, Joost M. Woltering, Iker Irisarri, Wai Yee Wong, Sergej Nowoshilow, Susanne Kneitz, Akane Kawaguchi, Anfrej Fabrizius, Peiwen Xiong, Corentin Dechaud, Herman P. Spaink, Jean-Nicolas Volff, Oleg Simakov, Thorsten Burmester, Elly M. Tanaka & Manfred Schartl
