Evolution after whole genome duplication: teleost microRNAs

• Published in: Molecular Biology and Evolution
• Main Authors: Desvignes, Thomas, Sydes, Jason, Montfort, Jerôme, Bobe, Julien, Postlethwait, John
• Other Authors: Institute of Neuroscience, University of Oregon, Eugene, Oregon, University of Oregon Eugene, Laboratoire de Physiologie et Génomique des Poissons = Fish Physiology and Genomics Institute (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), This work was supported by the National Institutes of Health (grant numbers NIH R24 OD011199, NIH 5R01 OD011116, and NIH R01 GM085318 to JHP), the National Science Foundation Office of Polar Program (NSF OPP-1543383 to JHP and TD), and Agence Nationale de la Recherche (ANR-18-CE20-0004 to JB). This work benefited from access to the University of Oregon high performance computers Talapas and ACISS (NSF grant OCI-0960354). Authors also thank Clayton M. Small for advises on statistical analyses and the handling editor and three anonymous reviewers for their helpful comments, ANR-18-CE20-0004,DynaMO,Elucider les bases cellulaires de la fécondité chez le poisson : dynamique et régulation de l'ovogenèse chez le medaka(2018)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2021
• Subjects: Chaenocephalus aceratus; Japanese medaka; Oryzias latipes; Spotted gar; Lepisosteus oculatus; Zebrafish; Danio rerio; Three-spined stickleback; Gasterosteus aculeatus; Blackfin icefish; arm-switching; [SDV]Life Sciences [q-bio]; [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics; Icefish
• Online Access: https://hal.inrae.fr/hal-03205656; https://hal.inrae.fr/hal-03205656/document; https://hal.inrae.fr/hal-03205656/file/2021_desvignes_MolBiolEvol.pdf; https://doi.org/10.1093/molbev/msab105

International audience microRNAs (miRNAs) are important gene expression regulators implicated in many biological processes, but we lack a global understanding of how miRNA genes evolve and contribute to developmental canalization and phenotypic diversification. Whole genome duplication events likely provide a substrate for species divergence and phenotypic change by increasing gene numbers and relaxing evolutionary pressures. To understand the consequences of genome duplication on miRNA evolution, we studied miRNA genes following the Teleost Genome Duplication (TGD). Analysis of miRNA genes in four teleosts and in spotted gar, whose lineage diverged before the TGD, revealed that miRNA genes were retained in ohnologous pairs more frequently than protein-coding genes, and that gene losses occurred rapidly after the TGD. Genomic context influenced retention rates, with clustered miRNA genes retained more often than non-clustered miRNA genes and intergenic miRNA genes retained more frequently than intragenic miRNA genes, which often shared the evolutionary fate of their protein-coding host. Expression analyses revealed both conserved and divergent expression patterns across species in line with miRNA functions in phenotypic canalization and diversification, respectively. Finally, major strands of miRNA genes experienced stronger purifying selection, especially in their seeds and 3’ complementary regions, compared to minor strands, which nonetheless also displayed evolutionary features compatible with constrained function. This study provides the first genome-wide, multi-species analysis of the mechanisms influencing metazoan miRNA evolution after whole genome duplication.