Skip to main content
SpringerLink
Log in

Transcriptome Analysis of Reciprocal Hybrids Between Crassostrea gigas and C. angulata Reveals the Potential Mechanisms Underlying Thermo-Resistant Heterosis

  • Research
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Heterosis, also known as hybrid vigor, is widely used in aquaculture, but the molecular causes for this phenomenon remain obscure. Here, we conducted a transcriptome analysis to unveil the gene expression patterns and molecular bases underlying thermo-resistant heterosis in Crassostrea gigas ♀ × Crassostrea angulata ♂ (GA) and C. angulata ♀ × C. gigas ♂ (AG). About 505 million clean reads were obtained, and 38,210 genes were identified, of which 3779 genes were differentially expressed between the reciprocal hybrids and purebreds. The global gene expression levels were toward the C. gigas genome in the reciprocal hybrids. In GA and AG, 95.69% and 92.00% of the differentially expressed genes (DEGs) exhibited a non-additive expression pattern, respectively. We observed all gene expression modes, including additive, partial dominance, high and low dominance, and under- and over-dominance. Of these, 77.52% and 50.00% of the DEGs exhibited under- or over-dominance in GA and AG, respectively. The over-dominance DEGs common to reciprocal hybrids were significantly enriched in protein folding, protein refolding, and intrinsic apoptotic signaling pathway, while the under-dominance DEGs were significantly enriched in cell cycle. As possible candidate genes for thermo-resistant heterosis, GRP78, major egg antigen, BAG, Hsp70, and Hsp27 were over-dominantly expressed, while MCM6 and ANAPC4 were under-dominantly expressed. This study extends our understanding of the thermo-resistant heterosis in oysters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this article and supplementary information.

References

  • Baranwal VK, Mikkilineni V, Zehr UB, Tyagi AK, Kapoor S (2012) Heterosis: emerging ideas about hybrid vigour. J Exp Bot 63:6309–6314

    Article  CAS  PubMed  Google Scholar 

  • Bi Y, Meyer A, Downs GS, Shi X, El-kereamy A, Lukens L, Rothstein SJ (2014) High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics 15:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley BA, Gracey AY, Somero GN (2006) The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J Exp Biol 209:2660–2677

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482

    Article  CAS  PubMed  Google Scholar 

  • Childs LH, Witucka-Wall H, Günther T, Sulpice R, von Korff M, Stitt M, Walther D, Schmid KJ, Altmann T (2010) Single feature polymorphism (SFP)-based selective sweep identification and association mapping of growth-related metabolic traits in Arabidopsis thaliana. BMC Genomics 11:188

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui X, Affourtit J, Shockley KR, Woo Y, Churchill GA (2006) Inheritance patterns of transcript levels in F1 hybrid mice. Genetics 174:627–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Lorgeril J, Lucasson A, Petton B, Toulza E, Montagnani C, Clerissi C, Vidal-Dupiol J, Chaparro C, Galinier R, Escoubas JM, Haffner P, Dégremont L, Charrière GM, Lafont M, Delort A, Vergnes A, Chiarello M, Faury N, Rubio T, Leroy MA, Pérignon A, Régler D, Morga B, Alunno-Bruscia M, Boudry P, Roux FL, Destoumieux-Garzόn D, Gueguen Y, Mitta G (2018) Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nat Commun 9:4215

    Article  PubMed  PubMed Central  Google Scholar 

  • de la Cruz FL, Gallardo-Escárate C (2011) Intraspecies and interspecies hybrids in Haliotis: natural and experimental evidence and its impact on abalone aquaculture. Rev Aquac 3:74–99

    Article  Google Scholar 

  • Debes PV, Normandeau E, Fraser DJ, Bernatchez L, Hutchings JA (2012) Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments. Mol Ecol 21:2574–2587

    Article  CAS  PubMed  Google Scholar 

  • Di G, Luo X, You W, Zhao J, Kong X, Ke C (2015) Proteomic analysis of muscle between hybrid abalone and parental lines Haliotis gigantea reeve and Haliotis discus hannai Ino. Heredity 114:564–574

  • Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiévet J, Dillmann C, de Vienne D (2010) Systemic properties of metabolic networks lead to an epistasis-based model for heterosis. Theor Appl Genet 120:463–473

    Article  PubMed  Google Scholar 

  • Fujimoto R, Taylora JM, Shirasawab S, Peacocka WJ, Dennisa ES (2012) Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci USA 109:7109–7114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Zhang H, Gao Q, Wang L, Zhang F, Siva VS, Zhou Z, Song L, Zhang S (2013) Transcriptome analysis of artificial hybrid pufferfish Jiyan-1 and its parental species: implications for pufferfish heterosis. PLoS One 8:e58453

  • Ghaffari H, Wang W, Li A, Zhang G, Li L (2019) Thermotolerance divergence revealed by the physiological and molecular responses in two oyster subspecies of Crassostrea gigas in China. Front Physiol 10:1137

    Article  PubMed  PubMed Central  Google Scholar 

  • Green RD (2009) Future needs in animal breeding and genetics. J Anim Sci 87:793–800

    Article  CAS  PubMed  Google Scholar 

  • Griffing B (1990) Use of a controlled-nutrient experiment to test heterosis hypotheses. Genetics 126:753–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu H, Qi Y, Jia Y, Zhang Z, Nie C, Li X, Li J, Jiang Z, Wang Q, Qu L (2019) Inheritance patterns of the transcriptome in hybrid chickens and their parents revealed by expression analysis. Sci Rep 9:4043

    Google Scholar 

  • Guo M, Rupe MA, Danilevskaya ON, Yang XF, Hu ZH (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36:30–44

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  CAS  PubMed  Google Scholar 

  • Hedgecock D, Lin J, DeCola S, Haudenschild CD, Meyer E, Manahan DT, Bowen B (2007) Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc Natl Acad Sci USA 104:2313–2318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Z, Feng J, Song H, Zhou C, Yu Z, Yang M, Shi P, Guo Y, Li Y, Zhang T (2022) Mechanisms of heat and hypoxia defense in hard clam: insights from transcriptome analysis. Aquaculture 549:737792

  • Jiang G, Li Q, Xu C, Liu S, Kong L, Yu H (2021) Reciprocal hybrids derived from Crassostrea gigas and C. angulata exhibit high heterosis in growth, survival and thermotolerance in northern China. Aquaculture 545:737173

  • Jiang G, Li Q, Xu C (2022a) Growth, survival and gonad development of two new types of reciprocal triploid hybrids between Crassostrea gigas and C. angulata. Aquaculture 559:738451

  • Jiang G, Zhou J, Cheng G, Meng L, Chi Y, Xu C, Li Q (2022b) Examination of survival, physiological parameters and immune response in relation to the thermo-resistant heterosis of hybrid oysters derived from Crassostrea gigas and C. angulata. Aquaculture 559:738454

  • Jörgensen PM, Gräslund S, Betz R, Ståhl S, Larsson C, Höög C (2001) Characterisation of the human APC1, the largest subunit of the anaphase-promoting complex. Gene 262:51–59

    Article  PubMed  Google Scholar 

  • Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463

    Article  CAS  PubMed  Google Scholar 

  • Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, Wang J (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 42:1027–1030

    Article  CAS  PubMed  Google Scholar 

  • Lampros M, Vlachos N, Voulgaris S, Alexiou GA (2022) The role of Hsp27 in chemotherapy resistance. Biomedicines 10:897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langdon C, Evans F, Jacobson D, Blouin M (2003) Yield of culture Pacific oyster Crassostrea gigas Thunberg improved after one generation of selection. Aquaculture 220:227–244

    Article  Google Scholar 

  • Li D, Huang Z, Song S, Xin Y, Mao D, Lv Q, Zhou M, Tian D, Tang M, Wu Q, Liu X, Chen T, Song X, Fu X, Zhao B, Liang C, Li A, Liu G, Li S, Hu S, Cao X, Yu J, Yuan L, Chen C, Zhu L (2016) Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase. Proc Natl Acad Sci USA 113:E6026–E6035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li A, Li L, Song K, Wang W, Zhang G (2017) Temperature, energy metabolism, and adaptive divergence in two oyster subspecies. Ecol Evol 7:6151–6162

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang S (2017) Physiological and molecular basis of cold disease resistance heterosis in Haliotis diversicolor hybrid. Xiamen University, Xiamen

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo Q, Samanta, MP, Köksal F, Janda J, Galbraith DW, Richardson CR, Ou-Yang F, Rock CD (2009) Evidence for antisense transcription associated with microRNA target mRNAs in Arabidopsis. PLoS Genet 5:e1000457

  • Meng L, Li Q, Xu C, Liu S, Kong L, Yu H (2021) Hybridization improved stress resistance in the Pacific oyster: evidence from physiological and immune responses. Aquaculture 545:737227

  • Rawson P, Feindel S (2012) Growth and survival for genetically improved lines of eastern oysters (Crassostrea virginica) and interline hybrids in Maine, USA. Aquaculture 25:61–67

    Article  Google Scholar 

  • Rao R, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE (2002) Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 514:122–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman MA, Arshad A, Marimuthu K, Ara R, Amin SMN (2013) Inter-specific hybridization and its potential for aquaculture of fin fishes. Asian J Anim Vet Adv 8:139–153

    Article  Google Scholar 

  • Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA 108:4069–4074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shatkin G, Shumway SE, Hawes R (1997) Considerations regarding the possible introduction of the Pacific oyster (Crassostrea gigas) to the Gulf of Maine: a review of global experience. J Shellfish Res 16:463–477

  • Somerville C, Somerville S (1999) Plant functional genomics. Science 285:380–383

    Article  CAS  PubMed  Google Scholar 

  • Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275

    Article  CAS  PubMed  Google Scholar 

  • Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 lead to additive expression patterns in the F1 hybrid. Genetics 173:2199–2210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Huang Y, Hu G, Zhang X, Ruan Z, Zhao X, Guo C, Tang Z, Li X, You X, Lin H, Zhang Y, Shi Q (2016) Comparative transcriptomic study of muscle provides new insights into the growth superiority of a novel grouper hybrid. PLoS One 11:e0168802

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810

  • Swanson-Wagner RA, DeCook R, Jia Y, Bancroft T, Ji T, Zhao X, Nettleton D, Schnable PS (2009) Paternal dominance of trans-eQTL influences gene expression patterns in maize hybrids. Science 326:1118–1120

    Article  CAS  PubMed  Google Scholar 

  • Tan K, Liu H, Ye T, Ma H, Li S, Zheng H (2020) Growth, survival and lipid composition of Crassostrea gigas, C. angulata and their reciprocal hybrids cultured in southern China. Aquaculture 516:734524

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripp-Valdez MA, Cicala F, Galindo-Sánchez CE, Chacón-Ponce KD, López-Landavery E, Díaz F, Re-Araujo D, Lafarga-De la Cruz F (2021) Growth performance and transcriptomic response of warm-acclimated hybrid abalone Haliotis rufescens (♀) × H. corrugata (♂). Mar Biotechnol 23:62–76

    Article  CAS  Google Scholar 

  • Vuylsteke M, Eeuwijk FV, Hummelen PV, Kuiper M, Zabeau M (2005) Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 171:1267–1275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Liu B, Li J, Liu S, Li J, Hu L, Fan X, Du H, Fang H (2011) Introduction of the Peruvian scallop and its hybridization with the bay scallop in China. Aquaculture 310:380–387

    Article  Google Scholar 

  • Xiao Q, Huang Z, Shen Y, Gan Y, Wang Y, Gong S, Lu Y, Luo X, You W, Ke C (2021) Transcriptome analysis reveals the molecular mechanisms of heterosis on thermal resistance in hybrid abalone. BMC Genomics 22:650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C (2013) Larch genes mining and mechanism on differential gene expression and heterosis formation. Chinese Academy of Forestry, Beijing

  • Yang J, Luo S, Li J, Zheng Z, Du X, Deng Y (2018) Transcriptome analysis of growth heterosis in pearl oyster Pinctada fucata martensii. FEBS Open Bio 8:1794–1803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng T, Guan Y, Li Y, Wu Q, Tang XJ, Zeng X, Ling H, Zou J (2021) The DNA replication regulator MCM6: an emerging cancer biomarker and target. Clin Chim Acta 517:92–98

    Article  CAS  PubMed  Google Scholar 

  • Zhai R, Feng Y, Wang H, Zhan X, Shen X, Wu W, Zhang Y, Chen D, Dai G, Yang Z, Cao L, Cheng S (2013) Transcriptome analysis of rice root heterosis by RNA-Seq. BMC Genomics 14:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Li J, Zhang J, Liang X, Zhang X, Wang T, Yi S (2019) Integrated analysis of transcriptomic, miRNA and proteomic changes of a novel hybrid yellow catfish uncovers key roles for miRNAs in heterosis. Mol Cell Proteomics 18:1437–1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xu X, He Z, Zheng T, Shao J (2017) De novo transcriptome analysis reveals insights into different mechanisms of growth and immunity in a Chinese soft-shelled turtle hybrid and the parental varieties. Gene 605:54–62

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Lin C, Fu F, Zhong X, Peng B, Yan H, Zhang J, Zhang W, Wang P, Ding X, Zhang W, Zhao L (2017b) Comparative transcriptome analysis of flower heterosis in two soybean F1 hybrids by RNA-seq. PLoS One 12: e0181061

  • Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PWH, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z, Zhu Q, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y, Domazet-Lošo T, Du Y, Sun X, Zhang S, Liu B, Cheng P, Jiang X, Li J, Fan D, Wang W, Fu W, Wang T, Wang B, Zhang J, Peng Z, Li Y, Li N, Wang J, Chen M, He Y, Tan F, Song X, Zheng Q, Huang R, Yang H, Du X, Chen L, Yang M, Gaffney PM, Wang S, Luo L, She Z, Ming Y, Huang W, Zhang S, Huang B, Zhang Y, Qu T, Ni P, Miao G, Wang J, Wang Q, Steinberg CEW, Wang H, Li N, Qian L, Zhang G, Li Y, Yang H, Liu X, Wang J, Yin Y, Wang J (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

  • Zhang L, Hou R, Su H, Hu X, Wang S, Bao Z (2012b) Network analysis of oyster transcriptome revealed a cascade of cellular responses during recovery after heat shock. PLoS One 7: e35484

  • Zhang J, Li R, Chen X, He X, Wang Z, Zheng Y, Hu J, Guo X (2021) Preparation of the major egg antigen recombinant protein of Echinococcus multilocularis and its preliminary application in immunodiagnosis. Chinese Veterin Sci 50:982–988

    Google Scholar 

  • Zhang X, Fan C, Zhang X, Li Q, Li Y, Ma P, Yue S, Huo Z, Wang Z (2022) Transcriptome analysis of Crassostrea sikamea (♀) × Crassostrea gigas (♂) hybrids under and after thermal stress. J Ocean Univ China 21:213–224

  • Zheng G, Wu C, Liu J, Chen J, Zou S (2019) Transcriptome analysis provides new insights into the growth superiority of a novel backcross variety, Megalobrama amblycephala ♀ × (M. amblycephala ♀ × Culter alburnus ♂) ♂. Aquaculture 512:734317

  • Zhou Y, Ren L, Xiao J, Zhong H, Wang J, Hu J, Yu F, Tao M, Zhang C, Liu Y, Liu S (2015) Global transcriptional and miRNA insights into bases of heterosis in hybridization of Cyprinidae. Sci Rep 5:13847

  • Zhu Q, Zhang L, Li L, Que H, Zhang G (2016) Expression characterization of stress genes under high and low temperature stresses in the Pacific oyster, Crassostrea gigas. Mar Biotechnol 18:176–188

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the grants from the China Agriculture Research System Project (CARS-49) and Earmarked Fund for Agriculture Seed Improvement Project of Shandong Province (2021LZGC027 and 2020LZGC016).

Author information

Authors and Affiliations

  1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Gaowei Jiang, Yin Li, Geng Cheng, Kunyin Jiang, Jianmin Zhou, Chengxun Xu, Lingfeng Kong, Hong Yu, Shikai Liu & Qi Li

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Qi Li

Authors
  1. Gaowei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Geng Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kunyin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianmin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chengxun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lingfeng Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shikai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Qi Li conceived and designed the study. Gaowei Jiang, Yin Li, Geng Cheng, Kunyin Jiang, and Jianmin Zhou performed the heat shock experiment and collected the samples. Gaowei Jiang, Yin Li, Kunyin Jiang, Chengxun Xu, Lingfeng Kong, Hong Yu, and Shikai Liu analyzed the data. Gaowei Jiang drafted the manuscript, and Qi Li revised the manuscript. All authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Qi Li.

Ethics declarations

Ethics Approval

The C. gigas, C. angulata, and their reciprocal hybrids are neither an endangered nor protected species. All experiments in this study were conducted according to national and institutional guidelines.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, G., Li, Y., Cheng, G. et al. Transcriptome Analysis of Reciprocal Hybrids Between Crassostrea gigas and C. angulata Reveals the Potential Mechanisms Underlying Thermo-Resistant Heterosis. Mar Biotechnol 25, 235–246 (2023). https://doi.org/10.1007/s10126-023-10197-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-023-10197-5

Keywords

Search

Navigation