Abstract
Understanding origin, evolution and functions of small RNA (sRNA) genes has been a great challenge in the past decade. Molecular mechanisms underlying sexual reversal in vertebrates, particularly sRNAs involved in this process, are largely unknown. By deep-sequencing of small RNA transcriptomes in combination with genomic analysis, we identified a large amount of piRNAs and miRNAs including over 1,000 novel miRNAs, which were differentially expressed during gonad reversal from ovary to testis via ovotesis. Biogenesis and expressions of miRNAs were dynamically changed during the reversal. Notably, phylogenetic analysis revealed dynamic expansions of miRNAs in vertebrates and an evolutionary trajectory of conserved miR-17-92 cluster in the Eukarya. We showed that the miR-17-92 cluster in vertebrates was generated through multiple duplications from ancestor miR-92 in invertebrates Tetranychus urticae and Daphnia pulex from the Chelicerata around 580 Mya. Moreover, we identified the sexual regulator Dmrt1 as a direct target of the members miR-19a and -19b in the cluster. These data suggested dynamic biogenesis and expressions of small RNAs during sex reversal and revealed multiple expansions and evolutionary trajectory of miRNAs from invertebrates to vertebrates, which implicate small RNAs in sexual reversal and provide new insight into evolutionary and molecular mechanisms underlying sexual reversal.
Highlights
The piRNAs are another abundant class of small ncRNAs, which are associated with PIWI proteins in germline[24,25,26,27,28]
After mapping to the reference genome, Rfam database, GenBank noncoding databases and repeat annotation files, the small RNAs were annotated and a full list of small RNAs involved in gonad reversal was obtained including tRNAs, snRNAs, miRNAs and piRNAs (Fig. 1b; Table S1)
1,524 pre-miRNAs encoding 1,274 mature miRNAs including 231 conserved and 1043 novel miRNAs were obtained (Fig. 1c,d; Table S2, S3); and 139,379, 166,903 and 249,000 unique piRNA sequences were detected in ovary, ovotestis and testis (Fig. 1e), respectively, indicating that both miRNAs and piRNAs are enriched in germline during gonad reversal
Summary
The piRNAs are another abundant class of small ncRNAs, which are associated with PIWI proteins in germline[24,25,26,27,28]. MiR-430 was a direct posttranscriptional regulator of sexual related genes nanos, tdrd[7], hub and sdf-1 which are necessary for the proper migration, maintenance and survival of primordial germ cells[49,50,51,52]. These studies highlight the importance of understanding the functions of miRNAs in germline development. We identified the sexual regulator Dmrt[1] as a direct target of the members miR-19a and -19b in the cluster These results provide new insight into the evolution and functions of miRNAs in sexual differentiation
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