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
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Sample Collection, Ploidy Verification, and Histology
2.3. RNA Extraction, Transcriptome Sequencing and Analysis
2.4. Proteome Sequencing and Analysis
2.4.1. Protein Extraction and Protein Digestion
2.4.2. Generation of the Spectral Library
2.4.3. Mass Spectrometry Data Analysis
2.4.4. Bioinformatics Analysis
2.5. Quantitative Real-Time PCR (qRT-PCR) Analysis
3. Results
3.1. Ploidy Verification, and Histological Observations of Gonadal Development in Diploid and Triploid Pacific Oysters
3.2. Proteins Identified in Gonads of C. gigas
3.3. Correlation Analysis of Transcriptome and Proteome in C. gigas
3.4. GO Enrichment Analysis between Fertile and Sterile Oysters
3.5. Key Pathways Related to Oyster Sterility Analysis by Proteome and Transcriptome
3.6. Validation of Selected DEGs
4. Discussion
4.1. Downregulation of Mitotic Cell Cycle-Related Genes May Be Associated with Sterility of Triploid Females
4.2. Downregulation of Genes Related to Cell Cycle and Sperm Motility in Sterile Male Triploids
4.3. Sterile Triploid Oysters Exhibited Increased Biosynthesis of Glycogen and Fat
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Van De Peer, Y.; Mizrachi, E.; Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 2017, 18, 411–424. [Google Scholar] [CrossRef]
- Bloom, S.E. Chromosome abnormalities in chicken (Gallus domesticus) embryos: Types, frequencies and phenotypic effects. Chromosoma 1972, 37, 309–326. [Google Scholar] [CrossRef] [PubMed]
- Hassold, T.; Hunt, P. To ERR (meiotically) is human: The genesis of human aneuploidy. Nat. Rev. Genet. 2001, 2, 280–291. [Google Scholar] [CrossRef] [PubMed]
- Leggatt, R.A.; Iwama, G.K. Occurrence of polyploidy in the fishes. Rev. Fish Biol. Fish. 2003, 13, 237–246. [Google Scholar] [CrossRef]
- Mable, B.K.; Alexandrou, M.A.; Taylor, M.I. Genome duplication in amphibians and fish: An extended synthesis. J. Zool. 2011, 284, 151–182. [Google Scholar] [CrossRef]
- Bogart, J.P.; Bi, K. Genetic and genomic interactions of animals with different ploidy levels. Cytogenet. Genome Res. 2013, 140, 117–136. [Google Scholar] [CrossRef]
- Manan, H.; Ikhwanuddin, M. Triploid induction in penaeid shrimps aquaculture: A review. Rev. Aquac. 2021, 13, 619–631. [Google Scholar] [CrossRef]
- Rasmussen, R.S.; Morrissey, M.T. Biotechnology in aquaculture: Transgenics and polyploidy. Compr. Rev. Food. Sci. Food Saf. 2007, 6, 2–16. [Google Scholar] [CrossRef]
- Francesc, P.; Andy, B.; Jean-Claude, F.; Martin, F.; Pierrick, H.; Lorenzo, C. Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 2009, 293, 125–156. [Google Scholar]
- Van der Zee, E.M.; van der, H.T.; Donadi, S.; Eklof, J.S.; Eriksson, B.K.; Olff, H.; van der Veer, H.W.; Piersma, T. Spatially Extended Habitat Modification by Intertidal Reef-Building Bivalves has Implications for Consumer-Resource Interactions. Ecosystems 2012, 15, 664–673. [Google Scholar] [CrossRef] [Green Version]
- Olivier, A.V.; Jones, L.; Le Vay, L.; Christie, M.; Wilson, J.; Malham, S.K. A global review of the ecosystem services provided by bivalve aquaculture. Rev. Aquac. 2020, 12, 3–25. [Google Scholar] [CrossRef] [Green Version]
- Vendrami, D.; Houston, R.D.; Gharbi, K.; Telesca, L.; Gutierrez, A.P.; Gurney-Smith, H.; Hasegawa, N.; Boudry, P.; Hoffman, J.I. Detailed insights into pan-European population structure and inbreeding in wild and hatchery Pacific oysters (Crassostrea gigas) revealed by genome-wide SNP data. Evol. Appl. 2019, 12, 519–534. [Google Scholar] [CrossRef] [Green Version]
- Guo, X.M.; Cooper, K.; Hershberger, W.K.; Chew, K.K. Genetic consequences of blocking polar body I with cytochalasin B in fertilized eggs of the Pacific oyster, Crassostrea gigas: I. ploidy of resultant embryos. Biol. Bull. 1992, 183, 381–386. [Google Scholar] [CrossRef] [PubMed]
- Kang, J.H.; Lim, H.J.; Kang, H.S.; Lee, J.M.; Baby, S.; Kim, J.J. Development of genetic markers for triploid verification of the Pacific oyster, Crassostrea Gigas. Asian Australas. J. Anim. Sci. 2013, 26, 916–920. [Google Scholar] [CrossRef] [Green Version]
- Stanley, J.G.; Allen Jr, S.K.; Hidu, H. Polyploidy induced in the American oyster, Crassostrea virginica, with cytochalasin B. Aquaculture 1981, 37, 1–10. [Google Scholar] [CrossRef]
- Guo, X.M.; DeBrosse, G.A.; Allen Jr, S.K. All-triploid Pacific oysters (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture 1996, 142, 149–161. [Google Scholar] [CrossRef]
- Allen Jr, S.K.; Downing, S.L. Performance of triploid Pacific oysters, Crassostrea gigas (Thunberg). I. Survival, growth, glycogen content, and sexual maturation in yearlings. J. Exp. Mar. Biol. Ecol. 1986, 102, 197–208. [Google Scholar] [CrossRef]
- Nell, J.A.; Perkins, B. Studies on triploid oysters in Australia: Farming potential of all-triploid Pacific oysters, Crassostrea gigas (Thunberg), in Port Stephens, New South Wales, Australia. Aquac. Res. 2005, 36, 530–536. [Google Scholar] [CrossRef]
- Wadsworth, P.; Wilson, A.E.; Walton, W.C. A meta-analysis of growth rate in diploid and triploid oysters. Aquaculture 2019, 499, 9–16. [Google Scholar] [CrossRef]
- Dégremont, L.; Garcia, C.; Allen Jr, S.K. Genetic improvement for disease resistance in oysters: A review. J. Invertebr. Pathol. 2015, 131, 226–241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garnier-Géré, P.H.; Naciri-Graven, Y.; Bougrier, S.; Magoulas, A.; Heral, M.; Kotoulas, G.; Hawkins, A.; Gerard, A. Influences of triploidy, parentage and genetic diversity on growth of the Pacific oyster Crassostrea gigas reared in contrasting natural environments. Mol. Ecol. 2002, 11, 1499–1514. [Google Scholar] [CrossRef] [Green Version]
- Guo, X.M. The development and commercialization of triploid oysters. In World Aquaculture; Sterility in Aquaculture-Advances, Performance, Impacts: Hawaii, HI, USA, 2020. [Google Scholar]
- Jouaux, A.; Heude-Berthelin, C.; Sourdaine, P.; Mathieu, M.; Kellner, K. Gametogenic stages in triploid oysters Crassostrea gigas: Irregular locking of gonial proliferation and subsequent reproductive effort. J. Exp. Mar. Biol. Ecol. 2010, 395, 162–170. [Google Scholar] [CrossRef]
- Matt, J.L.; Allen Jr, S.K. A classification system for gonad development in triploid Crassostrea virginica. Aquaculture 2021, 532, 735994. [Google Scholar] [CrossRef]
- Suquet, M.; Malo, F.; Quere, C.; Leduc, C.; Le Grand, J.; Benabdelmouna, A. Gamete quality in triploid Pacific oyster (Crassostrea gigas). Aquaculture 2016, 451, 11–15. [Google Scholar] [CrossRef] [Green Version]
- Dheilly, N.M.; Jouaux, A.; Boudry, P.; Favrel, P.; Lelong, C. Transcriptomic profiling of gametogenesis in triploid Pacific oysters Crassostrea gigas: Towards an understanding of partial sterility associated with triploidy. PLoS ONE 2014, 9, e112094. [Google Scholar] [CrossRef] [Green Version]
- Wang, R.; Wen, L.T.; Ma, H.W.; Lv, M.; Chen, Z.; Du, X.S.; Lin, Y.; Yang, H.Z. Effects of gonadotropin-releasing hormone analog (GnRHa) immunization on the gonadal transcriptome and proteome of tilapia (Oreochromis niloticus). Comp. Biochem. Physiol. D-Genom. Proteom. 2021, 37, 100780. [Google Scholar]
- Zhai, Y.F.; Dong, X.L.; Gao, H.H.; Chen, H.; Yang, P.Y.; Li, P.; Yin, Z.J.; Zheng, L.; Yu, Y. Quantitative proteomic and transcriptomic analyses of metabolic regulation of adult reproductive diapause in Drosophila suzukii (Diptera: Drosophilidae) Females. Front. Physiol. 2019, 10, 344. [Google Scholar] [CrossRef] [PubMed]
- Mateo Leach, I.; Hesseling, A.; Huibers, W.H.C.; Witsenboer, H.; Beukeboom, L.W.; van de Zande, L. Transcriptome and proteome analysis of ovaries of arrhenotokous and thelytokous Venturia canescens. Insect Mol. Biol. 2009, 18, 477–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zarski, D.; Le Cam, A.; Frohlich, T.; Kosters, M.; Klopp, C.; Nynca, J.; Ciesielski, S.; Sarosiek, B.; Dryl, K.; Montfort, J.; et al. Neurodevelopment vs. the immune system: Complementary contributions of maternally-inherited gene transcripts and proteins to successful embryonic development in fish. Genomics 2021, 113, 3811–3826. [Google Scholar] [CrossRef]
- Anders, S.; Huber, W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11, R106. [Google Scholar] [CrossRef] [Green Version]
- Vandesompele, J.; Preter, K.D.; Pattyn, F.; Poppe, B.; Roy, N.V.; Paepe, A.D.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Herpin, A.; Lelong, C.; Becker, T.; Favrel, P.; Cunningham, C. A tolloid homologue from the Pacific oyster Crassostrea Gigas. Gene Expr. Patterns 2007, 7, 700–708. [Google Scholar] [CrossRef] [PubMed]
- Du, Y.S.; Zhang, L.L.; Xu, F.; Huang, B.Y.; Zhang, G.F.; Li, L. Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative real-time PCR. Fish Shellfish. Immunol. 2013, 34, 939–945. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Harikae, K.; Miura, K.; Kanai, Y. Early gonadogenesis in mammals: Significance of long and narrow gonadal structure. Dev. Dyn. 2013, 242, 330–338. [Google Scholar] [CrossRef]
- Low, T.Y.; Mohtar, M.A.; Ang, M.Y.; Jamal, R. Connecting proteomics to nextgeneration sequencing: Proteogenomics and its current applications in biology. Proteomics 2019, 19, e1800235. [Google Scholar] [CrossRef] [PubMed]
- Ul Quraish, R.; Sudou, N.; Nomura-Komoike, K.; Sato, F.; Fujieda, H. p27(KIP1) loss promotes proliferation and phagocytosis but prevents epithelial-mesenchymal transition in RPE cells after photoreceptor damage. Mol. Vis. 2016, 22, 1103–1121. [Google Scholar] [PubMed]
- Santamaría, D.; Barrière, C.; Cerqueira, A.; Hunt, S.; Tardy, C.; Newton, K.; Cáceres, J.F.; Dubus, P.; Malumbres, M.; Barbacid, M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 2007, 448, 811–815. [Google Scholar] [CrossRef]
- Marston, A.L.; Amon, A. Meiosis: Cell-cycle controls shuffle and deal. Nat. Rev. Mol. Cell Biol. 2004, 5, 983–997. [Google Scholar] [CrossRef]
- Adhikari, D.; Zheng, W.J.; Shen, Y.; Gorre, N.; Ning, Y.; Halet, G.; Kaldis, P.; Liu, K. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum. Mol. Genet. 2012, 21, 2476–2484. [Google Scholar] [CrossRef] [Green Version]
- Løkkegaard, S.; Elias, D.; Alves, C.L.; Bennetzen, M.V.; Lænkholm, A.-V.; Bak, M.; Gjerstorff, M.F.; Johansen, L.E.; Vever, H.; Bjerre, C.; et al. MCM3 upregulation confers endocrine resistance in breast cancer and is a predictive marker of diminished tamoxifen benefit. NPJ Breast Cancer 2021, 7, 1–15. [Google Scholar] [CrossRef]
- Tye, B.K. MCM proteins in DNA replication. Annu. Rev. Biochem. 1999, 68, 649–686. [Google Scholar] [CrossRef]
- Takei, Y.; Tsujimoto, G. Identification of a novel MCM3-associated protein that facilitates MCM3 nuclear localization. J. Biol. Chem. 1998, 273, 22177–22180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stewart, P.A.; Khamis, Z.I.; Zhau, H.E.; Duan, P.; Li, Q.; Chung, L.W.K.; Sang, Q.A. Upregulation of minichromosome maintenance complex component 3 during epithelial-to-mesenchymal transition in human prostate cancer. Oncotarget 2017, 8, 39209–39217. [Google Scholar] [CrossRef]
- Ooi, W.F.; Re, A.; Sidarovich, V.; Canella, V.; Arseni, N.; Adami, V.; Guarguaglini, G.; Giubettini, M.; Scaruffi, P.; Stigliani, S.; et al. Segmental chromosome aberrations converge on overexpression of mitotic spindle regulatory genes in high-risk neuroblastoma. Gene Chromosomes Cancer 2012, 51, 545–556. [Google Scholar] [CrossRef] [PubMed]
- Pournoor, E.; Mousavian, Z.; Dalini, A.N.; Masoudi-Nejad, A. Identification of key components in colon adenocarcinoma using transcriptome to interactome multilayer framework. Sci. Rep. 2020, 10, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Y.H.; Bai, W.J.; Zhang, J.J. MiR-200c-5p suppresses proliferation and metastasis of human hepatocellular carcinoma (HCC) via suppressing MAD2L1. Biomed. Pharmacother. 2017, 92, 1038–1044. [Google Scholar] [CrossRef] [PubMed]
- Li, J.F.; He, X.; Wu, X.T.; Liu, X.H.; Huang, Y.X.; Gong, Y.C. miR-139-5p inhibits lung adenocarcinoma cell proliferation, migration, and invasion by targeting MAD2L1. Comput. Math. Method Med. 2020, 2020, 1–10. [Google Scholar] [CrossRef]
- Yang, Y.; Ding, L.L.; Zhou, Q.; Fen, L.; Cao, Y.H.; Sun, J.J.; Zhou, X.F.; Liu, A.G. Silencing of AURKA augments the antitumor efficacy of the AURKA inhibitor MLN8237 on neuroblastoma cells. Cancer Cell Int. 2020, 20, 9–16. [Google Scholar] [CrossRef]
- Senese, S.; Zaragoza, K.; Minardi, S.; Muradore, I.; Ronzoni, S.; Passafaro, A.; Bernard, L.; Draetta, G.F.; Alcalay, M.; Seiser, C.; et al. Role for Histone Deacetylase 1 in Human Tumor Cell Proliferation. Mol. Cell. Biol. 2007, 27, 4784–4795. [Google Scholar] [CrossRef] [Green Version]
- Glaser, K.B.; Li, J.L.; Staver, M.J.; Wei, R.Q.; Albert, D.H.; Davidsen, S.K. Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem. Biophys. Res. Commun. 2003, 310, 529–536. [Google Scholar] [CrossRef]
- Nishioka, C.; Ikezoe, T.; Yang, J.; Takeuchi, S.; Koeffler, H.P.; Yokoyama, A. MS-275, a novel histone deacetylase inhibitor with selectivity against HDAC1, induces degradation of FLT3 via inhibition of chaperone function of heat shock protein 90 in AML cells. Leuk. Res. 2008, 32, 1382–1392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, P.P.; Pan, H.; Montgomery, R.L.; Olson, E.N.; Schultz, R.M. Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc. Natl. Acad. Sci. USA 2012, 109, E481–E489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ortega, S.; Prieto, I.; Odajima, J.; Martín, A.; Dubus, P.; Sotillo, R.; Barbero, J.L.; Malumbres, M.; Barbacid, M. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 2003, 35, 25–31. [Google Scholar] [CrossRef]
- Vogel, P.; Read, R.W.; Hansen, G.M.; Payne, B.J.; Small, D.; Sands, A.T.; Zambrowicz, B.P. Congenital hydrocephalus in genetically engineered mice. Vet. Pathol. 2012, 49, 166–181. [Google Scholar] [CrossRef]
- Nagarkatti-Gude, D.R.; Jaimez, R.; Henderson, S.C.; Teves, M.E.; Zhang, Z.B.; Strauss, J.F. Spag16, an axonemal central apparatus gene, encodes a male germ cell nuclear speckle protein that regulates SPAG16 mRNA expression. PLoS ONE 2011, 6, e20625. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, S.; Li, L.; Meng, J.; Song, K.; Huang, B.Y.; Wang, W.; Zhang, G.F. Association and functional analyses revealed that PPP1R3B plays an important role in the regulation of glycogen content in the Pacific oyster Crassostrea gigas. Front. Genet. 2019, 10, 106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kioumourtzoglou, D.; Pryor, P.R.; Gould, G.W.; Bryant, N.J. Alternative routes to the cell surface underpin insulin-regulated membrane trafficking of GLUT4. J. Cell Sci. 2015, 128, 2423–2429. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shan, D.D.; Li, J.L.; Wu, L.Y.; Li, D.M.; Hurov, J.; Tobin, J.F.; Gimeno, R.E.; Cao, J.S. GPAT3 and GPAT4 are regulated by insulin-stimulated phosphorylation and play distinct roles in adipogenesis. J. Lipid Res. 2010, 51, 1971–1981. [Google Scholar] [CrossRef] [Green Version]
- Barber, B.; Blake, N.J. Intra-organ biochemical transformations associated with oogenesis in the bay scallop, Argopecten irradians concentricus (Say), as indicated by 14C incorporation. Biol. Bull. 1985, 168, 39–49. [Google Scholar] [CrossRef]
- Wang, S.; Xue, M.Y.; Yang, Q.; Yu, H.; Li, Q. Comparison of nutritional components of different fertility triploid Pacific oyster (Crassostrea gigas) during gonadal development. J. Fish. China 2021, 45, 88–97. [Google Scholar]
Name | Sequences (5′ to 3′) | Product Size (bp) | Amplification Efficiency (%) |
---|---|---|---|
CDK1_F | ACTGGCAGACTTTGGATTGG | 85 | 93.7 |
CDK1_R | GGCTCTGTACCATAGCGTCA | ||
MCM3_F | ATGACAAGTGCCGTCTCGTT | 198 | 103.6 |
MCM3_R | CACCAAAGCTGCCCTCAAAC | ||
GPAT4_F | CACACGTCTCCACTGGATGT | 93 | 109.6 |
GPAT4_R | CATGACCAGTCCCAGGAACC | ||
Slc2a4_F | TGGGCGTGTCCAAACTCT | 154 | 101.5 |
Slc2a4_R | CTGGCTTCTTCCTCTTCATTCT | ||
MAD2L1_F | TCCGTCACATTCCTACCC | 140 | 95.5 |
MAD2L1_R | CGCAGTCTCACTTCCTCC | ||
EIF3B_F | ATGATGTCGGAAACCTGC | 147 | 95.6 |
EIF3B_R | CAGTCCACCTTGCTCTTT | ||
AURKA_F | AGTTCTTTCATCCGGGCACT | 147 | 104.2 |
AURKA_R | TGGCTCTTTCCTGCTTGGTT | ||
mcm7_F | GATGGAGGGTGACAGAACCG | 101 | 95.9 |
mcm7_R | TGGAGACCCTAGCGTTGAGA | ||
SPAG16_F | TGCCCTAGCAACATCTCAGA | 189 | 92 |
SPAG16_R | ACCACTCCGATGTCCTCCTC | ||
NME5_F | GCCATAGTGATAGCAAGAGACCA | 130 | 91.3 |
NME5_R | TGCGCTGATCATCTGTTCCA | ||
AK7_F | AGCCAAGACGAAGAGAAGCC | 156 | 92.4 |
AK7_R | GCTGGTGGTTGACCTAGCAT | ||
EF-1α_F | AGTCACCAAGGCTGCACAGAAAG | 200 | 100.2 |
EF-1α_R | TCCGACGTATTTCTTTGCGATGT | ||
GAPDH_F | TTCTCTTGCCCCTCTTGC | 127 | 99.9 |
GAPDH_R | CGCCCAATCCTTGTTGCTT | ||
RO21_F | AATGCCAGGCTAACAGACCACA | 100 | 93.2 |
RO21_R | TTGGATTTCTGAGATTCCGATCTTC | ||
RS18_F | GCCATCAAGGGTATCGGTAGAC | 168 | 99.1 |
RS18_R | CTGCCTGTTAAGGAACCAGTCAG | ||
RL7_F | TCCCAAGCCAAGGAAGGTTATGC | 242 | 101.7 |
RL7_R | CAAAGCGTCCAAGGTGTTTCTCAA |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chen, C.; Yu, H.; Li, Q. 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). Cells 2021, 10, 2668. https://doi.org/10.3390/cells10102668
Chen C, Yu H, Li Q. 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). Cells. 2021; 10(10):2668. https://doi.org/10.3390/cells10102668
Chicago/Turabian StyleChen, Chen, Hong Yu, and Qi Li. 2021. "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)" Cells 10, no. 10: 2668. https://doi.org/10.3390/cells10102668
APA StyleChen, C., Yu, H., & Li, Q. (2021). 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). Cells, 10(10), 2668. https://doi.org/10.3390/cells10102668