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Heritability of resistance-related gene expression traits and their correlation with body size of clam Meretrix petechialis

  • Aquaculture and Fisheries
  • Published:
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Abstract

Gene expression variation can be considered as a phenotype, and it plays an important role in both acclimation and adaption. However, genetic variation of gene expression received much less attention than traditional commercial traits in aquaculture. To estimate the genetic variation and heritability of gene transcription in clam Meretrix petechialis, five Vibrio resistance-related genes were selected for gene expression analysis in the digestive gland, and an animal linear model was used to analyze data from quantitative real-time PCR (qRT-PCR). Among the five genes, BIRC7 showed significant additive genetic variations, the heritability of this gene of 12-month- and 15-month-old clams were 0.84±0.32 and 0.91±0.34, respectively. The heritability of other four genes (Bax, NFIL3, Big-Def, and CTL9) expression were low-to-moderate but not significantly expressed. Additionally, no significant phenotypic and genetic correlations between the BIRC7 transcription trait and body size were detected. This study highlights that certain gene expression variation is heritable and provides a reference for indirect selection of M. petechialis with high Vibrio resistance.

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Data Availability Statement

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study. All data generated and/or analyzed during this study are included in this published article.

Abbreviations

Bax:

apoptosis regulator Bax

BIRC7:

baculoviral IAP repeat-containing protein 7 isoform X3

Big-Def:

Big defensing

CTL9:

C-type lectin 9

NFIL3:

nuclear factor interleukin-3-regulated protein

References

  • Antonello J, Massault C, Franch R, Haley C, Pellizzari C, Bovo G, Patarnello T, De Koning D J, Bargelloni L. 2009. Estimates of heritability and genetic correlation for body length and resistance to fish pasteurellosis in the gilthead sea bream (Sparus aurata L.). Aquaculture298 (1-2): 29–35.

    Google Scholar 

  • Aykanat T, Heath J W, Dixon B, Heath D D. 2012. Additive, non-additive and maternal effects of cytokine transcription in response to immunostimulation with Vibrio vaccine in Chinook salmon (Oncorhynchus tshawytscha). Immunogenetics, 64 (9): 691–703.

    Google Scholar 

  • Ayroles J F, Carbone M A, Stone E A, Jordan K W, Lyman R F, Magwire M M, Rollmann S M, Duncan L H, Lawrence F, Anholt R R, Mackay T F. 2009. Systems genetics of complex traits in Drosophila melanogaster Nature Genetics, 41 (3): 299–307.

    Google Scholar 

  • Bangera R, Ødegård J, Præbel A K, Mortensen A, Nielsen H M. 2011. Genetic correlations between growth rate and resistance to vibriosis and viral nervous necrosis in Atlantic cod (Gadus morhua L.). Aquaculture, 317 (1-4): 67–73.

    Google Scholar 

  • Berg P, Henryon M. 1999. Selection response under alternative mating designs in fish. Proc Adv Anim Breed Gen., 13: 297–300.

    Google Scholar 

  • Bishop S C, Woolliams J A. 2014. Genomics and disease resistance studies in livestock. Livestock Science166: 190–198.

    Google Scholar 

  • Brokordt K B, González R C, Farías W J, Winkler F M. 2015. Potential response to selection of HSP70 as a component of innate immunity in the abalone Haliotis rufescens PLoS One, 10 (11): e0141959.

    Google Scholar 

  • Cheung V G, Spielman R S. 2002. The genetics of variation in gene expression. Nature Genetics, 32 (S4): 522–525.

    Google Scholar 

  • Crawford D L, Powers D A. 1992. Evolutionary adaptation to different thermal environments via transcriptional regulation. Molecular Biology and Evolution9 (5): 806–813.

    Google Scholar 

  • Dixon A L, Liang L M, Moffatt M F, Chen W, Heath S, Wong K C C, Taylor J, Burnett E, Gut I, Farrall M, Lathrop G M, Abecasis G R, Cookson W O. 2007. A genome-wide association study of global gene expression. Nature Genetics, 39 (10): 1 202–1 207.

    Google Scholar 

  • Engwerda C R, Kaye P M. 2000. Organ-specific immune responses associated with infectious disease. Immunology Today, 21 (2): 73–78.

    Google Scholar 

  • Evans M L, Neff B D. 2009. Non-additive genetic effects contribute to larval spinal deformity in two populations of Chinook salmon (Oncorhynchus tshawytscha). Aquaculture, 296 (1-2): 169–173.

    Google Scholar 

  • Flores-Mara R, Rodríguez F H, Bangera R, Lhorente J P, Neira R, Newman S, Yáñez J M. 2017. Resistance against infectious pancreatic necrosis exhibits significant genetic variation and is not genetically correlated with harvest weight in rainbow trout (Oncorhynchus mykiss). Aquaculture, 479: 155–160.

    Google Scholar 

  • Gao X G, He C B, Liu H, Li H J, Zhu D, Cai S L, Xia Y, Wang Y, Yu Z. 2012. Intracellular Cu/Zn superoxide dismutase (Cu/Zn-SOD) from hard clam Meretrix meretrix: its cDNA cloning, mRNA expression and enzyme activity. Molecular Biology Reports, 39 (12): 10 713–10 722.

    Google Scholar 

  • Gilad Y, Rifkin S A, Pritchard J K. 2008. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends in Genetics, 24 (8): 408–415.

    Google Scholar 

  • Gilmour A R, Gogel B, Cullis B, Thompson R, Butler D. 2009. ASReml User Guide Release 3.0. VSN International Ltd., Hemel Hempstead, UK.

    Google Scholar 

  • He X, Houde A L S, Pitcher T E, Heath D D. 2017. Genetic architecture of gene transcription in two Atlantic salmon (Salmo salar) populations. Heredity (Edinb)119 (2): 117–124.

    Google Scholar 

  • Houle D, Govindaraju D R, Omholt S. 2010. Phenomics: the next challenge. Nature Reviews Genetics11 (12): 855–866.

    Google Scholar 

  • Jiang F J, Wang H X, Yue X, Zhang S J, Liu B Z. 2018. Integrating the Vibrio-resistance phenotype and gene expression data for discovery of markers used for resistance evaluation in the clam Meretrix petechialis Aquaculture, 482: 130–136.

    Google Scholar 

  • Jiang F J, Yue X, Wang H X, Liu B Z. 2017. Transcriptome profiles of the clam Meretrix petechialis hepatopancreas in response to Vibrio infection. Fish & Shellfish Immunology, 62: 175–183.

    Google Scholar 

  • Langevin C, Blanco M, Martin S A, Jouneau L, Bernardet J F, Houel A, Lunazzi A, Duchaud E, Michel C, Quillet E, Boudinot P. 2012. Transcriptional responses of resistant and susceptible fish clones to the bacterial pathogen Flavobacterium psychrophilum PLoS One7 (6): e39126.

    Google Scholar 

  • Lavine M D, Strand M R. 2002. Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32 (10): 1 295–1 309.

    Google Scholar 

  • Leder E H, McCairns R J, Leinonen T, Cano J M, Viitaniemi H M, Nikinmaa M, Primmer C R, Merilä J. 2015. The evolution and adaptive potential of transcriptional variation in sticklebacks—signatures of selection and widespread heritability. Molecular Biology and Evolution32 (3): 674–689.

    Google Scholar 

  • Liang B B, Jiang F J, Zhang S J, Yue X, Wang H X, Liu B Z. 2017. Genetic variation in vibrio resistance in the clam Meretrix petechialis under the challenge of Vibrio parahaemolyticus. Aquaculture, 468: 458–463.

    Google Scholar 

  • Liu B Z, Dong B, Tang B J, Zhang T, Xiang J H. 2006. Effect of stocking density on growth, settlement and survival of clam larvae, Meretrix meretrix Aquaculture258 (1-3): 344–349.

    Google Scholar 

  • Marancik D, Gao G T, Paneru B, Ma H, Hernandez A G, Salem M, Yao J B, Palti Y, Wiens G D. 2014. Whole-body transcriptome of selectively bred, resistant-, control-, and susceptible-line rainbow trout following experimental challenge with Flavobacterium psychrophilum Front Genetiers, 5: 453.

    Google Scholar 

  • Nie Q, Yue X, Chai X L, Wang H X, Liu B Z. 2013. Three vibrio-resistance related EST-SSR markers revealed by selective genotyping in the clam Meretrix meretrix Fish & Shellfish Immunology, 35 (2): 421–428.

    Google Scholar 

  • Nie Q, Yue X, Liu B Z. 2015. Development of Vibrio spp. infection resistance related SNP markers using multiplex SNaPshot genotyping method in the clam Meretrix meretrix. Fish & Shellfish Immunology, 43 (2): 469–476.

    Google Scholar 

  • Normandeau E, Hutchings J A, Fraser D J, Bernatchez L. 2009. Population-specific gene expression responses to hybridization between farm and wild Atlantic salmon. Evolutionary Applications, 2 (4): 489–503.

    Google Scholar 

  • PfafflM W. 2001. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research, 29 (9): e45.

    Google Scholar 

  • Powell J E, Henders A K, McRae A F, Kim J, Hemani G, Martin N G, Dermitzakis E T, Gibson G, Montgomery G W, Visscher P M. 2013. Congruence of additive and nonadditive effects on gene expression estimated from pedigree and SNP data. PLoS Genetics, 9 (5): e1003502.

    Google Scholar 

  • Reyes-López F E, Romeo J S, Vallejos-Vidal E, Reyes-Cerpa S, Sandino A M, Tort L, Mackenzie S, Imarai M. 2015. Differential immune gene expression profiles in susceptible and resistant full-sibling families of Atlantic salmon (Salmo salar) challenged with infectious pancreatic necrosis virus (IPNV). Developmental & Comparative Immunology, 53 (1): 210–221.

    Google Scholar 

  • Roberge C, Guderley H, Bernatchez L. 2007. Genomewide identification of genes under directional selection: gene transcription QST scan in diverging Atlantic salmon subpopulations. Genetics, 177 (2): 1 011–1 022.

    Google Scholar 

  • Robinson N, Hayes B. 2008. Modelling the use of gene expression profiles with selective breeding for improved disease resistance in Atlantic salmon (Salmo salar). Aquaculture, 285 (1-4): 38–46.

    Google Scholar 

  • Robledo D, Taggart J B, Ireland J H, McAndrew B J, Starkey W G, Haley C S, Hamilton A, Guy D R, Mota-Velasco J C, Gheyas A A, Tinch A E, Verner-Jeffreys D W, Paley R K, Rimmer G S, Tew I J, Bishop S C, Bron J E, Houston R D. 2016. Gene expression comparison of resistant and susceptible Atlantic salmon fry challenged with Infectious Pancreatic Necrosis virus reveals a marked contrast in immune response. BMC Genomics, 17: 279.

    Google Scholar 

  • Röszer T. 2014. The invertebrate midintestinal gland (“hepatopancreas”) is an evolutionary forerunner in the integration of immunity and metabolism. Cell and Tissue Research, 358 (3): 685–695.

    Google Scholar 

  • Silverstein J T, Vallejo R L, Palti Y, Leeds T D, Rexroad III C E, Welch T J, Wiens G D, Ducrocq V. 2009. Rainbow trout resistance to bacterial cold-water disease is moderately heritable and is not adversely correlated with growth. Journal of Animal Science, 87 (3): 860–867.

    Google Scholar 

  • Tedeschi J N, Kennington W J, Tomkins J L, Berry O, Whiting S, Meekan M G, Mitchell N J. 2016. Heritable variation in heat shock gene expression: a potential mechanism for adaptation to thermal stress in embryos of sea turtles. Proceedings Biological Sciences, 283 (1822): 20152320.

    Google Scholar 

  • Wang H X, Chai X L, Liu B Z. 2011. Estimation of genetic parameters for growth traits in cultured clam Meretrix meretrix (Bivalvia: Veneridae) using the Bayesian method based on Gibbs sampling. Aquaculture Research42 (2): 240–247.

    Google Scholar 

  • Whitehead A, Crawford D L. 2006. Variation within and among species in gene expression: raw material for evolution. Molecular Ecology, 15 (5): 1 197–1 211.

    Google Scholar 

  • Yáñez J M, Bangera R, Lhorente J P, Barría A, Oyarzún M, Neira R, Newman S. 2016. Negative genetic correlation between resistance against Piscirickettsia salmonis and harvest weight in coho salmon (Oncorhynchus kisutch). Aquaculture, 459: 8–13.

    Google Scholar 

  • Yang J, Benyamin B, McEvoy B P, Gordon S, Henders A K, Nyholt D R, Madden P A, Heath A C, Martin N G, Montgomery G W, Goddard M E, Visscher P M. 2010. Common SNPs explain a large proportion of the heritability for human height. Nature Genetics42 (7): 565–569.

    Google Scholar 

  • Zou L H, Liu B Z. 2016. The polymorphisms of a MIF gene and their association with Vibrio resistance in the clam Meretrix meretrix Developmental & Comparative Immunology, 62: 116–126.

    Google Scholar 

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Correspondence to Hongxia Wang.

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Supported by the China Agriculture Research System (No. CARS-49), the National Natural Science Foundation of China (No. 31772845), the Science and Technology Service Network Initiative of the Chinese Academy of Sciences (No. KFJ-STS-ZDTP-049), and the Foundation of Zhejiang Key Laboratory of Exploitation and Preservation of Coastal Bio-Resource (No. J2018001)

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Jiang, F., Yue, X., Zhang, S. et al. Heritability of resistance-related gene expression traits and their correlation with body size of clam Meretrix petechialis. J. Ocean. Limnol. 38, 571–578 (2020). https://doi.org/10.1007/s00343-019-8326-3

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  • DOI: https://doi.org/10.1007/s00343-019-8326-3

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