Evolution after Whole-Genome Duplication: Teleost MicroRNAs

Abstract

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.

Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout

“…In addition, existing studies in rainbow trout often rely on miRNA annotations available in other species (e.g., Atlantic salmon) [ 25 ] as no rainbow trout miRNA annotation is available in miRBase [ 35 ] and other databases [ 36 ]. Finally, the rainbow trout miRNAome annotation reported here is consistent with the recently described evolution of miRNA genes in teleost fish [ 29 ]. While slightly lower, the number of mature rainbow trout miRNAs reported here is in agreement with previous reports in other ray-finned fish species using similar genome-wide annotation strategies that led to the annotation of 362, 495, 396, and 408 individual mature miRNAs in gar, zebrafish, stickleback, and icefish, respectively [ 30 – 32 ].…”

“…Rainbow trout was chosen due to its relatively large size, which simplifies the fluid collection, its belonging to the economically and culturally important salmonid family, as well as its sequenced genome and available small RNA-seq data in 38 different tissues, cell types, organs, and embryonic stages [ 28 ]. In fish, a comprehensive view of the overall miRNA repertoire was only recently characterized [ 29 ] but was still lacking in rainbow trout. We thus established a comprehensive annotation of expressed miRNAs in rainbow trout using existing and newly generated sRNA-seq data and using existing miRNAome annotations in teleost fish [ 30 – 34 ].…”

MicroRNAs as Indicators into the Causes and Consequences of Whole-Genome Duplication Events

“…Aside from the studies of Bhambri et al (2018) and Desvignes et al (2021) , most efforts to understand the increase in miRNA paralog numbers in metazoan taxa that have undergone WGD events ( Hertel et al 2006 ; Berthelot et al 2014 ; Braasch et al 2016 ; Leite et al 2016 ; Shingate, Ravi, Prasad, Tay, Garg, et al 2020 ; Nong et al 2021 ) were hampered by the difficulty in assigning direct homology between individual miRNA genes. However, MirGeneDB ( Fromm et al 2015 , 2020 ) was created with the specific intent to use a consistent nomenclature system that explicitly recognizes paralogs within a taxon and orthologs across taxa based on both syntenic and phylogenetic analyses.…”

“…2 A , white bar). The teleost fish Danio rerio though has up seven paralogs of miRNAs due to the 3R event that occurred in the teleost lineage after it split from the holostean fish like the gar, but before the teleost LCA ( Glasauer and Neuhauss 2014 ; Desvignes et al 2021 ). For miRNA families that evolved after 2R, but before 3R, these occur at no more than two times in the genome of D. rerio ( fig.…”

Leafy and Weedy Seadragon Genomes Connect Genic and Repetitive DNA Features to the Extravagant Biology of Syngnathid Fishes

“…These absences include mir130a, mir301a, mir130b, mir301b, mir130c-2, and mir454b. While mir130a, mir301a, and mir301b are convergently missing in platyfish (X. maculatus) and medaka (O. latipes), absences of mir130b, mir130c-2, and mir454b have not yet been reported in other vertebrate species (Figure S18) (Desvignes et al, 2019;Desvignes et al, 2021;Kelley et al, 2021). In some tetrapods and teleosts, mir301a is located in the first intron of ska2.…”