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Comparative transcriptome analysis of abalone Haliotis discus hannai with green and gray egg colors

  • Aquaculture and Fisheries
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Abstract

Haliotis discus hannai is an important marine economic species in China. Its egg color was found to be associated with economic traits, which provides a new idea for breeding. However, the molecular mechanism of the egg-color formation has not been reported. Thus, the pigment composition and comparative transcriptome analyses of H. discus hannai with green and gray egg color were conducted using high-performance liquid chromatography (HPLC) and RNA-Seq methods. Results show that individuals with green and gray eggs both possess the fucoxanthin. Lutein existed in gray-egged individuals, but not in green-egged individuals. In transcriptome analysis, 272 310 unigenes were received from 461 162 transcripts with a mean length of 985 bp and N50 of 1 524 bp, respectively. A total of 185 unigenes were identified as differentially expressed genes (DEGs). The DEGs involved in “flavin-containing compound metabolic process”, “melanosome”, “glutathione metabolism”, and “cytochrome b6f complex” were likely related to the formation of the egg color. Our results provide foundational information for the functional analysis of egg-color related genes and are beneficial to the selective breeding of H. discus hannai.

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References

  • Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403–410, https://doi.org/10.1016/S0022.2836(05)80360-2.

    Article  Google Scholar 

  • Apweiler R, Bairoch A, Wu C H, Barker W C, Boeckmann B, Ferro S, Gasteiger E, Huang H Z, Lopez R, Magrane M Martin M J, Natale D A, O’Donovan C, Redaschi N, Yeh L S L. 2004. UniProt: the Universal Protein knowledgebase. Nucleic Acids Research, 32(S1): D115–D119, https://doi.org/10.1093/nar/gkh131.

    Article  Google Scholar 

  • Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Issel-Tarver L, Kasarskis A, Lewis S, Matese J C, Richardson J E, Ringwald M, Rubin G M, Sherlock G. 2000. Gene ontology: tool for the unification of biology. Nature Genetics, 25(1): 25–29, https://doi.org/10.1038/75556.

    Article  Google Scholar 

  • Cassan N, Lagoutte B, Sétif P. 2005. Ferredoxin-NADP+ Reductase kinetics of electron transfer, transient intermediates, and catalytic activities studied by flashabsorption spectroscopy with isolated photosystem I and ferredoxin. Journal of Biological Chemistry, 280(28): 25960–25972, https://doi.org/10.1074/jbc.M503742200.

    Article  Google Scholar 

  • Choi M J, Kim G D, Kim J M, Lim H K. 2015. Differentially-expressed genes associated with faster growth of the Pacific abalone, Haliotis discus hannai. International Journal of Molecular Sciences, 16(11): 27520–27534, https://doi.org/10.3390/ijms161126042.

    Article  Google Scholar 

  • Chu H L, Wang B S, Duh P D. 2009. Effects of selected organo-sulfur compounds on melanin formation. Journal of Agricultural and Food Chemistry, 57(15): 7072–7077, https://doi.org/10.1021/jf9005824.

    Article  Google Scholar 

  • Cooley J M. 1971. The effect of temperature on the development of resting eggs of Diaptomus oregonensis Lillj (Copepoda: Calanoida). Limnology and Oceanography, 16(6): 921–926, https://doi.org/10.4319/lo.1971.16.6.0921.

    Article  Google Scholar 

  • Couto N, Malys N, Gaskell S J, Barber J. 2013. Partition and turnover of glutathione reductase from Saccharomyces cerevisiae: a proteomic approach. Journal of Proteome Research, 12(6): 2885–2894, https://doi.org/10.1021/pr4001948.

    Article  Google Scholar 

  • Deng S Z, Zhang X L, Li Q C, Zhang J, Han F, Liu X D. 2018. Comparative transcriptome analysis of Paphia undulata with different foot colors. Marine Genomics, 42: 25–31, https://doi.org/10.1016/j.margen.2018.08.007.

    Article  Google Scholar 

  • Deng Y Y, Li J Q, Wu S F, Zhu Y P, Chen Y W, He F C. 2006. Integrated nr database in protein annotation system and its localization. Computer Engineering, 32(5): 71–73, 76. (in Chinese with English abstract)

    Google Scholar 

  • Ding J, Zhao L, Chang Y Q, Zhao W M, Du Z L, Hao Z L. 2015. Transcriptome sequencing and characterization of Japanese scallop Patinopecten yessoensis from different shell color lines. PLoS One, 10(2): e0116406, https://doi.org/10.1371/journal.pone.0116406.

    Article  Google Scholar 

  • Finn R D, Bateman A, Clements J, Coggill P, Eberhardt R Y, Eddy S R, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer E L L, Tate J, Punta M. 2013. Pfam: the protein families database. Nucleic Acids Research, 42(D1): D222–D230, https://doi.org/10.1093/nar/gkt1223.

    Article  Google Scholar 

  • Gordon H R, Cook P A. 2004. World abalone fisheries and aquaculture update: supply and market dynamics. Journal of Shellfish Research, 23(4): 935–939.

    Google Scholar 

  • Guo H, Ye C X, Wang A L, Xian J A, Liao S A, Miao Y T, Zhang S P. 2013. Trascriptome analysis of the Pacific white shrimp Litopenaeus vannamei exposed to nitrite by RNA-seq. Fish & Shellfish Immunology, 35(6): 2008–2016, https://doi.org/10.1016/j.fsi.2013.09.019.

    Article  Google Scholar 

  • Harney E, Dubief B, Boudry P, Basuyaux O, Schilhabel M B, Huchette S, Paillard C, Nunes F L D. 2016. De novo assembly and annotation of the European abalone Haliotis tuberculata transcriptome. Marine Genomics, 28: 11–16, https://doi.org/10.1016/j.margen.2016.03.002.

    Article  Google Scholar 

  • Holmgren A, Johansson C, Berndt C, Lönn M E, Hudemann C, Lillig C H. 2005. Thiol redox control via thioredoxin and glutaredoxin systems. Biochemical Society Transactions, 33(6): 1375–1377, https://doi.org/10.1042/BST0331375.

    Article  Google Scholar 

  • Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter M C, Rattei T, Mende D R, Sunagawa S, Kuhn M Jensen L J, von Mering C, Bork P. 2015. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Research, 44(D1): D286–D293, https://doi.org/10.1093/nar/gkv1248.

    Article  Google Scholar 

  • Hulet R M, Marquez B J, Molle E, Flegal C J. 1978. Relationship of pheasant egg color and hatchability. Poultry Science, 57(4): 1146–1148.

    Google Scholar 

  • Jeukens J, Renaut S, ST-CYR J, Nolte A W, Bernatchez L. 2010. The transcriptomics of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis spp., Salmonidae) divergence as revealed by next-generation sequencing. Molecular Ecology, 19(24): 5389–5403, https://doi.org/10.1111/j.1365-294X.2010.04934.x.

    Article  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Research, 32(S1): D277–D280, https://doi.org/10.1093/nar/gkh063.

    Article  Google Scholar 

  • Kim M A, Rhee J S, Kim T H, Lee J S, Choi A Y, Choi B S, Choi I Y, Sohn Y C. 2017. Alternative splicing profile and sex-preferential gene expression in the female and male Pacific Abalone Haliotis discus hannai. Genes, 8(3): 99, https://doi.org/10.3390/genes8030099.

    Article  Google Scholar 

  • Koch P B, Behnecke B, Weigmann-Lenz M, Ffrench-Constant R H. 2000. Insect pigmentation: activities of ß, alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus. Pigment Cell Research, 13(S8): 54–58, https://doi.org/10.1111/j.0893-5785.2000.130811.x.

    Article  Google Scholar 

  • Leng X J, Li X Q. 2006. The recent advance of aquatic animal pigmentation. Journal of Fisheries of China, 30(1): 138–143. (in Chinese with English abstract)

    Google Scholar 

  • Li B, Dewey C N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1): 323.

    Article  Google Scholar 

  • Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1754–1760, https://doi.org/10.1093/bioinformatics/btp324.

    Article  Google Scholar 

  • Liang P X, Li Y R. 2016. Cloning of cytochrome b6-f complex iron-sulfur subunit (SoCYT) from sugarcane and analysis of its expression under PEG stress. Southwest China Journal of Agricultural Sciences, 29(5): 1032–1037, https://doi.org/10.16213/j.cnki.scjas.2016.05.008. (in Chinese with English abstract)

    Google Scholar 

  • Liu J H, Wang A L, Wang W N, Liu F S. 2002. Progress of study on the component of pigment and painting substance of aquatic animals. Chinese Journal of Zoology, 37(3): 92–96, https://doi.org/10.13859/j.cjz.2002.03.024. (in Chinese with English abstract)

    Google Scholar 

  • Liu Z Q, Lin S, Baker P J, Wu L F, Wang X R, Wu H, Xu F, Wang H Y, Brathwaite M E, Zheng Y G. 2015. Transcriptome sequencing and analysis of the entomopathogenic fungus Hirsutella sinensis isolated from Ophiocordyceps sinensis. BMC Genomics, 16(1): 106, https://doi.org/10.1186/s12864-015-1269-y.

    Article  Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods, 25(4): 402–408, https://doi.org/10.1006/meth.2001.1262.

    Google Scholar 

  • Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics, 21(19): 3787–3793, https://doi.org/10.1093/bioinformatics/bti430.

    Article  Google Scholar 

  • Metzker M L. 2010. Sequencing technologies-the next generation. Nature Reviews Genetics, 11(1): 31–46, https://doi.org/10.1038/nrg2626.

    Article  Google Scholar 

  • Nam B H, Jung M, Subramaniyam S, Yoo S I, Markkandan K, Moon J Y, Kim Y O, Kim D G, An C M, Shin Y, Jung H J, Park J H. 2016. Transcriptome analysis revealed changes of multiple genes involved in Haliotis discus hannai innate immunity during Vibrio parahemolyticus infection. PLoS One, 11(4): e0153474, https://doi.org/10.1371/journal.pone.0153474.

    Article  Google Scholar 

  • Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini A F. 2003. The changing faces of glutathione, a cellular protagonist. Biochemical Pharmacology, 66(8): 1499–1503, https://doi.org/10.1016/S0006-2952(03)00504-5.

    Article  Google Scholar 

  • Raposo G, Marks M S. 2007. Melanosomes—dark organelles enlighten endosomal membrane transport. Nature Reviews Molecular Cell Biology, 8(10): 786–797, https://doi.org/10.1038/nrm2258.

    Article  Google Scholar 

  • Shen Y W, Huang Z K, Liu G M, Ke C H, You W W. 2019. Hemolymph and transcriptome analysis to understand innate immune responses to hypoxia in Pacific abalone. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 30: 102–112, https://doi.org/10.1016/j.cbd.2019.02.001.

    Google Scholar 

  • Staehelin L A, Arntzen C J. 1983. Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. The Journal of Cell Biology, 97(5): 1327–1337, https://doi.org/10.1083/jcb.97.5.1327.

    Article  Google Scholar 

  • Symonds J E, Moss G, Jopson N B, Roberts R, Birss J, Heath P, Walkera S P, Andersonf R M, McEwan K M, Amer P R. 2012. Family-based selective breeding of New Zealand abalone, Haliotis iris: challenges and opportunities. Proceedings of the New Zealand Society of Animal Production, 72: 216–221.

    Google Scholar 

  • Tempest D W, Meers J L, Brown C M. 1970. Synthesis of glutamate in Aerobacter aerogenes by a hitherto unknown route. Biochemical Journal, 117(2): 405–407, https://doi.org/10.1042/bj1170405.

    Article  Google Scholar 

  • Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, Van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5): 511–515, https://doi.org/10.1038/nbt.1621.

    Article  Google Scholar 

  • Valenzuela-Miranda D, Del Río-Portilla M A, Gallardo-Escárate C. 2015. Characterization of the growth-related transcriptome in California red abalone (Haliotis rufescens) through RNA-Seq analysis. Marine Genomics, 24: 199–202, https://doi.org/10.1016/j.margen.2015.05.009.

    Article  Google Scholar 

  • Wang C H, Wachholtz M, Wang J, Liao X L, Lu G Q. 2014. Analysis of the skin transcriptome in two Oujiang color varieties of common carp. PLoS One, 9(3): e90074, https://doi.org/10.1371/journal.pone.0090074.

    Article  Google Scholar 

  • Wang L B. 2012. Effect of natural xanthophylls on growth performance, skin coloring and antioxidant function in yellow catfish (Pelteobagrus fulvidraco) and its metabolic regulation in fish tissues. Chinese Academy of Agricultural Sciences, Beijing. (in Chinese with English abstract)

    Google Scholar 

  • Wang S. 2015. Study on the selection of reference genes and the expression regulation of C-type lectin gene in Haliotis discus hannai. Shanghai Ocean University, Shanghai. (in Chinese with English abstract)

    Google Scholar 

  • Xing L L, Sun L N, Liu S L, Li X N, Miao T, Zhang L B, Yang H S. 2017. Comparison of pigment composition and melanin content among white, light-green, dark-green, and purple morphs of sea cucumber, Apostichopus japonicus. Acta Oceanologica Sinica, 36(12): 45–51, https://doi.org/10.1007/s13131-017-1056-5.

    Article  Google Scholar 

  • Xing L L, Sun L N, Liu S L, Li X N, Zhang L B, Yang H S. 2018. De Novo assembly and comparative transcriptome analyses of purple and green morphs of Apostichopus japonicus during body wall pigmentation process. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 28: 151–161, https://doi.org/10.1016/j.cbd.2018.09.001.

    Google Scholar 

  • You W W, Ke C H, Luo X, Wang D X, 2009. Growth and survival of three small abalone Haliotis diversicolor populations and their reciprocal crosses. Aquaculture Research, 40(13): 1474–1480, https://doi.org/10.1111/j.1365-2109.2009.02247.x.

    Article  Google Scholar 

  • Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology, 11(2): R14, https://doi.org/10.1186/gb-2010-11-2-r14.

    Article  Google Scholar 

  • Zhang H, Whitelegge J P, Cramer W A. 2001. Ferredoxin: NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. Journal of Biological Chemistry, 276(41): 38159–38165, https://doi.org/10.1074/jbc.M105454200.

    Article  Google Scholar 

  • Zhang X, Shi J L, Sun Y L, Habib Y J, Yang H P, Zhang Z P, Wang Y L. 2019. Integrative transcriptome analysis and discovery of genes involving in immune response of hypoxia/thermal challenges in the small abalone Haliotis diversicolor. Fish & Shellfish Immunology, 84: 609–626, https://doi.org/10.1016/j.fsi.2018.10.044.

    Article  Google Scholar 

  • Zhao H F, Feng Y W, Liu X Q, Jiang X, Wei X M, Liu J L. Jiang H L. 2016. Growth and immune diversity of Haliotis discus hannai juvenile abalone with different egg colors. Progress in Fishery Sciences, 37(6): 110–114, https://doi.org/10.11758/yykxjz.20150810001. (in Chinese with English abstract)

    Google Scholar 

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Correspondence to Yanwei Feng or Xiangquan Liu.

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All data that support the findings of this study are available from the corresponding author on reasonable request.

Supported by the Seed Improvement Project of Shandong Province of China (No. 2017LZGC009) and the Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (No. 2019JZZY020706)

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Feng, Y., Yuan, B., Jiang, X. et al. Comparative transcriptome analysis of abalone Haliotis discus hannai with green and gray egg colors. J. Ocean. Limnol. 39, 350–361 (2021). https://doi.org/10.1007/s00343-020-9302-7

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