Proteome and Transcriptome Analysis of Ovary, Intersex Gonads, and Testis Reveals Potential Key Sex Reversal/Differentiation Genes and Mechanism in Scallop Chlamys nobilis
- 140 Downloads
Bivalve mollusks exhibit hermaphroditism and sex reversal/differentiation. Studies generally focus on transcriptional profiling and specific genes related to sex determination and differentiation. Few studies on sex reversal/differentiation have been reported. A combination analysis of gonad proteomics and transcriptomics was conducted on Chlamys nobilis to provide a systematic understanding of sex reversal/differentiation in bivalves. We obtained 4258 unique peptides and 93,731 unigenes with good correlation between messenger RNA and protein levels. Candidate genes in sex reversal/differentiation were found: 15 genes differentially expressed between sexes were identified and 12 had obvious sexual functions. Three novel genes (foxl2, β-catenin, and sry) were expressed highly in intersex individuals and were likely involved in the control of gonadal sex in C. nobilis. High expression of foxl2 or β-catenin may inhibit sry and activate 5-HT receptor and vitellogenin to maintain female development. High expression of sry may inhibit foxl2 and β-catenin and activate dmrt2, fem-1, sfp2, sa6, Amy-1, APCP4, and PLK to maintain male function. High expression of sry, foxl2, and β-catenin in C. nobilis may be involved in promoting and maintaining sex reversal/differentiation. The downstream regulator may not be dimorphic expressed genes, but genes expressed in intersex individuals, males and females. Different expression patterns of sex-related genes and gonadal histological characteristics suggested that C. nobilis may change its sex from male to female. These findings suggest highly conserved sex reversal/differentiation with diverged regulatory pathways during C. nobilis evolution. This study provides valuable genetic resources for understanding sex reversal/differentiation (intersex) mechanisms and pathways underlying bivalve reproductive regulation.
KeywordsProteome Transcriptome Sex reversal/differentiation Intersex individual Chlamys nobilis
We would like to thank the Shanghai Applied Protein Technology Co., Ltd. for providing the technical support.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- Anderson K, Burnell FJ, Roiko A, Andrew M, Connor WAO, Elizur A (2010) Development of a method for identifying elevated vitellogenin gene expression in the Sydney rock oyster (Saccostrea glomerata) as an indicator of endocrine disruption on the Sunshine Coast. Ecol Manag Restor 11:143–146CrossRefGoogle Scholar
- Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 1999:138–148Google Scholar
- Li HL, Zhang ZF, Bi Y, Yang DD, Zhang LT, Liu JG (2014) Expression characteristics of beta-catenin in scallop Chlamys farreri gonads and its role as a potential upstream gene of Dax1 through canonical Wnt signalling pathway regulating the spermatogenesis. PLoS One 9:e115917CrossRefPubMedPubMedCentralGoogle Scholar
- Teaniniuraitemoana V, Huvet A, Levy P, Klopp C, Lhuillier E, Gaertner-Mazouni N, Gueguen Y, Le Moullac G (2014) Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes. BMC Genomics 15:491CrossRefPubMedPubMedCentralGoogle Scholar
- Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O’Kelly G, Schoenegger A, Ovelleiro D, Perez-Riverol Y, Reisinger F, Rios D, Wang R, Hermjakob H (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41:D1063–D1069CrossRefPubMedGoogle Scholar
- Wang YP, Zhou LS, Zhao YZ, Wang SW, Chen LL, Liu LX, Ling ZQ, Hu FJ, Sun YP, Zhang JY, Yang C, Yang Y, Xiong Y, Guan KL, Ye D (2014) Regulation of G6PD acetylation by SIRT2 and KAT9 modulates NADPH homeostasis and cell survival during oxidative stress. EMBO J 33:1304–1320PubMedPubMedCentralGoogle Scholar
- Williams VN, Reading BJ, Hiramatsu N, Amano H, Glassbrook N, Hara A, Sullivan CV (2014) Multiple vitellogenins and product yolk proteins in striped bass, Morone saxatilis: molecular characterization and processing during oocyte growth and maturation. Fish Physiol Biochem 40:395–415CrossRefPubMedGoogle Scholar
- Zhang Z, Tang WX, Zhou R, Shen XN, Wei ZY, Patel AM, Povlishock JT, Bennett J, Strauss JF (2007) Accelerated mortality from hydrocephalus and pneumonia in mice with a combined deficiency of SPAG6 and SPAG16L reveals a functional interrelationship between the two central apparatus proteins. Cell Motil Cytoskeleton 64:360–376CrossRefPubMedGoogle Scholar
- Zhang N, Xu F, Guo XM (2014) Genomic analysis of the Pacific oyster (Crassostrea gigas) reveals possible conservation of vertebrate sex determination in a mollusc. G3-Genes Genom Genet 4:2207–2217Google Scholar