Whole transcriptome RNA sequencing provides novel insights into the molecular dynamics of ovarian development in mud crab, Scylla paramamosain after mating
Yang Yu , Mengqian Zhang , Dahe Wang , Zifei Xiang , Zilin Zhao , Wenxiao Cui , Shaopan Ye , Hanafiah Fazhan , Khor Waiho , Mhd Ikhwanuddin , Hongyu Ma
{"title":"Whole transcriptome RNA sequencing provides novel insights into the molecular dynamics of ovarian development in mud crab, Scylla paramamosain after mating","authors":"Yang Yu , Mengqian Zhang , Dahe Wang , Zifei Xiang , Zilin Zhao , Wenxiao Cui , Shaopan Ye , Hanafiah Fazhan , Khor Waiho , Mhd Ikhwanuddin , Hongyu Ma","doi":"10.1016/j.cbd.2024.101247","DOIUrl":null,"url":null,"abstract":"<div><p>Ovarian development in animals is a complicated biological process, requiring the simultaneous coordination among various genes and pathways. To understand the dynamic changes and molecular regulatory mechanisms of ovarian development in mud crab (<em>Scylla paramamosain</em>), both histological observation and whole transcriptome sequencing of ovarian tissues at different mating stages were implemented in this study. The histological results revealed that ovarian development was delayed in unmated females (60 days after courtship behavior but not mating), who exhibited an oocyte diameter of 56.38 ± 15.17 μm. Conversely, mated females exhibited accelerated the ovarian maturation process, with females reaching ovarian stage III (proliferative stage) 23 days after mating and attained an average oocyte diameter of 132.19 ± 15.07 μm. Thus, mating process is essential in promoting the rapid ovarian development in mud crab. Based on the whole transcriptome sequencing analysis, a total of 518 mRNAs, 1502 lncRNAs, 18 circRNAs and 151 miRNAs were identified to be differentially expressed between ovarian tissues at different mating stages. Notably, six differentially expressed genes (DEGs) associated with ovarian development were identified, including <em>ovary development-related protein</em>, <em>red pigment concentrating hormone receptor</em>, <em>G2/mitotic-specific cyclin-B3-like</em>, <em>lutropin-chorio gonadotropic hormone receptor</em>, <em>renin receptor</em>, and <em>SoxB2</em>. More importantly, both DEGs and targets of differentially expressed non-coding RNAs (DEncRNAs) were enriched in renin-angiotensin system, TGF-β signaling, cell adhesion molecules, MAPK signaling pathway, and ECM-receptor interaction, suggesting that these pathways may play significant roles in the ovarian development of mud crabs. Moreover, competition endogenous RNA (ceRNA) networks were constructed while mRNAs were differentially expressed between mating stages were involved in Gene Ontology (GO) biological processes such as developmental process, reproduction, and growth. These findings could provide solid foundations for the future development of female mud crab maturation enhancement strategy, and improve the understanding of the ovarian maturation process in crustaceans.</p></div>","PeriodicalId":55235,"journal":{"name":"Comparative Biochemistry and Physiology D-Genomics & Proteomics","volume":"51 ","pages":"Article 101247"},"PeriodicalIF":2.2000,"publicationDate":"2024-05-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Comparative Biochemistry and Physiology D-Genomics & Proteomics","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1744117X24000601","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Ovarian development in animals is a complicated biological process, requiring the simultaneous coordination among various genes and pathways. To understand the dynamic changes and molecular regulatory mechanisms of ovarian development in mud crab (Scylla paramamosain), both histological observation and whole transcriptome sequencing of ovarian tissues at different mating stages were implemented in this study. The histological results revealed that ovarian development was delayed in unmated females (60 days after courtship behavior but not mating), who exhibited an oocyte diameter of 56.38 ± 15.17 μm. Conversely, mated females exhibited accelerated the ovarian maturation process, with females reaching ovarian stage III (proliferative stage) 23 days after mating and attained an average oocyte diameter of 132.19 ± 15.07 μm. Thus, mating process is essential in promoting the rapid ovarian development in mud crab. Based on the whole transcriptome sequencing analysis, a total of 518 mRNAs, 1502 lncRNAs, 18 circRNAs and 151 miRNAs were identified to be differentially expressed between ovarian tissues at different mating stages. Notably, six differentially expressed genes (DEGs) associated with ovarian development were identified, including ovary development-related protein, red pigment concentrating hormone receptor, G2/mitotic-specific cyclin-B3-like, lutropin-chorio gonadotropic hormone receptor, renin receptor, and SoxB2. More importantly, both DEGs and targets of differentially expressed non-coding RNAs (DEncRNAs) were enriched in renin-angiotensin system, TGF-β signaling, cell adhesion molecules, MAPK signaling pathway, and ECM-receptor interaction, suggesting that these pathways may play significant roles in the ovarian development of mud crabs. Moreover, competition endogenous RNA (ceRNA) networks were constructed while mRNAs were differentially expressed between mating stages were involved in Gene Ontology (GO) biological processes such as developmental process, reproduction, and growth. These findings could provide solid foundations for the future development of female mud crab maturation enhancement strategy, and improve the understanding of the ovarian maturation process in crustaceans.
期刊介绍:
Comparative Biochemistry & Physiology (CBP) publishes papers in comparative, environmental and evolutionary physiology.
Part D: Genomics and Proteomics (CBPD), focuses on “omics” approaches to physiology, including comparative and functional genomics, metagenomics, transcriptomics, proteomics, metabolomics, and lipidomics. Most studies employ “omics” and/or system biology to test specific hypotheses about molecular and biochemical mechanisms underlying physiological responses to the environment. We encourage papers that address fundamental questions in comparative physiology and biochemistry rather than studies with a focus that is purely technical, methodological or descriptive in nature.