Abstract

Simple SummaryThis study reveals the expression profiles of lncRNA in the gonads of the Pacific oyster Crassostrea gigas. The potential function of lncRNAs was predicted in the case of antisense and cis-regulatory mechanisms based on their physical positions and their coexpression relationships in the case of trans regulation. Sterility-related DEGs and DELs were chosen for subsequent analysis, demonstrating that trans-regulatory lncRNAs might play a vital role in the gametogenesis of C. gigas. We constructed core networks of lncRNAs–mRNAs for triploid sterile females and hermaphrodites based on pathway results, in which 28 lncRNAs and their 54 trans-regulatory genes were detected. Among 28 sterility-specific lncRNAs, MSTRG.79882.3 and MSTRG.79882.4 for triploid sterile females and MSTRG.33704.1, MSTRG.63844.1, and MSTRG.5675.1 for hermaphrodites play the most significant role.Long noncoding RNA (lncRNA), a type of non-protein-coding transcript, is emerging as a crucial regulator of gene expression. However, few roles of lncRNA in the reproductive process of the Pacific oyster (Crassostrea gigas) have been defined, especially in the regulatory mechanism of sterile triploids gametogenesis. To uncover the potential role of lncRNA, the gonads of diploids, sterile triploids, and partially sterile triploids underwent RNA sequencing. A total of 9618 reliable lncRNAs were identified. The target relationship between lncRNA and mRNA was predicted based on cis, trans, and antisense regulation with bioinformatic software. We chose differentially expressed lncRNAs and mRNAs when sterile triploids were compared to partially sterile triploids and diploids for subsequent functional enrichment analysis. Findings revealed that trans-regulatory lncRNAs might play a significant role in the gametogenesis of C. gigas. Combining pathway results, we constructed core networks of lncRNAs–mRNAs for triploid sterile females and hermaphrodites. Fifty-four genes related to cell division, germline-cell maintenance, and glycogen metabolism were found to be associated with sterility. A total of 28 candidate lncRNAs were predicted to trans-regulate these genes. We speculated that MSTRG.79882.3 and MSTRG.79882.4 for triploid sterile females and MSTRG.33704.1, MSTRG.63844.1, and MSTRG.5675.1 for hermaphrodites were highly important as they were predicted to regulate more sterility-specific genes than others. Our work collectively identified sterility-related lncRNAs and implicated the potential mechanism of lncRNA-mediated regulation in the gametogenesis of sterile triploid oysters.

Highlights

  • IntroductionGametogenesis is an integral part of the reproductive process, in which germ cells undergo proliferation and differentiation, thereby releasing their genetic information to the creativecommons.org/licenses/by/ 4.0/)

  • We focused on trans regulation, combining functional pathway results to establish core networks of Long noncoding RNA (lncRNA)–mRNAs in three groups

  • The present study demonstrated that downregulated cell-cycle-related genes related to trans-lncRNAs above might contribute to gametogenesis arrest of triploids

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Summary

Introduction

Gametogenesis is an integral part of the reproductive process, in which germ cells undergo proliferation and differentiation, thereby releasing their genetic information to the creativecommons.org/licenses/by/ 4.0/). Triploids need to overcome meiosis abnormalities during gametogenesis because of a redundant set of chromosomes [1]. Most aquaculture triploids of great commercial value have been reported to be sterile, and triploids could represent an interesting model for studies on gametogenesis. LncRNAs are RNA transcripts longer than 200 nucleotides that are not translated into polypeptides. Based on their loci and relationship with the functional genes on the chromosome, lncRNAs are classified as intronic, intergenic, sense, bidirectional, and antisense [2]. Antisense long noncoding RNAs (antisense-lncRNAs), as a sub-class of lncRNAs transcribed from the antisense of a proteincoding strand, have been broadly investigated [4]

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