Integrated Proteomic and Transcriptomic Analysis of Gonads Reveal Disruption of Germ Cell Proliferation and Division, and Energy Storage in Glycogen in Sterile Triploid Pacific Oysters (Crassostrea gigas)

Abstract

Triploid oysters have poor gonadal development, which can not only bring higher economic benefits but also have a potential application in the genetic containment of aquaculture. However, the key factors that influence germ cell development in triploid oysters remain unclear. In this study, data-independent acquisition coupled to transcriptomics was applied to identify genes/proteins related to sterility in triploid Crassostrea gigas. Eighty-four genes were differentially expressed at both the protein and mRNA levels between fertile and sterile females. For male oysters, 207 genes were differentially expressed in the transcriptomic and proteomic analysis. A large proportion of downregulated genes were related to cell division, which may hinder germ cell proliferation and cause apoptosis. In sterile triploid females, a primary cause of sterility may be downregulation in the expression levels of certain mitotic cell cycle-related genes. In sterile triploid males, downregulation of genes related to cell cycle and sperm motility indicated that the disruption of mitosis or meiosis and flagella defects may be linked with the blocking of spermatogenesis. Additionally, the genes upregulated in sterile oysters were mainly associated with the biosynthesis of glycogen and fat, suggesting that sterility in triploids stimulates the synthesis of glycogen and energy conservation in gonad tissue.

Transcription Analysis for Core Networks of lncRNAs–mRNAs: Implication for Potential Role in Sterility of Crassostrea gigas

“…[55]. This result echoed a previous report that flagella defects may be linked with spermatogenesis blocking [17]. MSTRG.5675.1 was predicted to interact with 6 genes of 17 unique DEGs in the HM-3n group, indicating it could play an important role.…”

“…Yue et al [15] reported that CgBHMG1, a factor involved in meiosis, was aberrantly expressed in the gonad of triploids. Further, transcriptomic and proteomic analysis results unveiled that cell-division-related genes were downregulated in sterile oysters, while the genes involved in nutrient biosynthesis and cell apoptosis were upregulated [16,17]. It confirmed that energy-metabolism difference and cell cycle arrest, to some extent, do induce sterility of C. gigas.…”

“…These DEGs were also mapped into KEGG pathways, and the top 20 statistically significant KEGG classifications are shown in Figure 4. Transcriptomic analysis of C. gigas unveiled that cell cycle and energy conservation difference was the primary cause of triploid sterility [17]. Given that, we focused on significantly enriched KEGG terms of interest.…”

Combined ATAC-seq, RNA-seq, and GWAS analysis reveals glycogen metabolism regulatory network in Jinjiang oyster (<i>Crassostrea ariakensis</i>)

“…This observation is in alignment with the distinct phases of oyster gonadal development, notably diverging in the mature and proligerous stages relative to other developmental stages ( Figure 1A ), implying that these DEGs are intricately linked to the process of gonadal development. As gonadal development has been shown to correlate with glycogen content in oysters ( Chen et al, 2021a ; Liu et al, 2020 ; Qin et al, 2021 ), the observed expression patterns also correlated with the glycogen phenotypes of these groups, whereby glycogen content was higher in groups 1, 2, and 5 than in groups 3 and 4. Consequently, the identified DEGs are likely associated with glycogen content in oysters.…”

“…For example, using transcriptomics, Wang et al ( 2021b ) identified several non-coding RNAs (ncRNAs) in the gonads of C. gigas postulated to indirectly regulate the expression of genes involved in glycogen metabolism, including protein phosphatase 1 regulatory subunit 3b ( ppp1r3b ), isocitrate dehydrogenase 1 ( idh1 ), and β-glucosidase. In addition, based on transcriptomics and metabolomics, Chen et al ( 2021a ) identified several genes related to glycogen metabolism, including glycogen synthase ( gys ), solute carrier family 2 member 4 ( slc2a4 ), and glycerol-3-phosphate acyltransferase 4 ( gpat4 ). These findings highlight the feasibility and efficiency of multi-omics technologies in screening genes related to quality traits of aquatic products.…”