Cite this paper:
Yanwei FENG, Bo YUAN, Xu JIANG, Xiangquan LIU, Zan LI, Guohua SUN, Xiaohui XU. Comparative transcriptome analysis of abalone Haliotis discus hannai with green and gray egg colors[J]. Journal of Oceanology and Limnology, 2021, 39(1): 350-361

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

Yanwei FENG1, Bo YUAN2,3,4, Xu JIANG5, Xiangquan LIU2, Zan LI1, Guohua SUN1, Xiaohui XU1
1 School of Agriculture, Ludong University, Yantai 264025, China;
2 Shandong Provincial Key Laboratory of Restoration for Marine Ecology, Shandong Marine Resource and Environment Research Institute, Yantai 264006, China;
3 National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China;
4 Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China;
5 Shandong Rice Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, China
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.
Key words:    Haliotis discus hannai|egg color|high-performance liquid chromatography|transcriptome|differentially expressed genes   
Received: 2019-12-06   Revised: 2020-01-26
Tools
PDF (2339 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Yanwei FENG
Articles by Bo YUAN
Articles by Xu JIANG
Articles by Xiangquan LIU
Articles by Zan LI
Articles by Guohua SUN
Articles by Xiaohui XU
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.
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.
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.
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):25 960-25 972, https://doi.org/10.1074/jbc.M503742200.
Choi M J, Kim G D, Kim J M, Lim H K. 2015. Differentiallyexpressed genes associated with faster growth of the Pacific abalone, Haliotis discus hannai. International Journal of Molecular Sciences, 16(11):27 520-27 534, https://doi.org/10.3390/ijms161126042.
Chu H L, Wang B S, Duh P D. 2009. Effects of selected organosulfur compounds on melanin formation. Journal of Agricultural and Food Chemistry, 57(15):7 072-7 077, https://doi.org/10.1021/jf9005824.
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.
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):2 885-2 894, https://doi.org/10.1021/pr4001948.
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.
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)
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.
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.
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.
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):2 008-2 016, https://doi.org/10.1016/j.fsi.2013.09.019.
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.
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):1 375-1 377, https://doi.org/10.1042/BST0331375.
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.
Hulet R M, Marquez B J, Molle E, Flegal C J. 1978.Relationship of pheasant egg color and hatchability.Poultry Science, 57(4):1 146-1 148.
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):5 389-5 403, https://doi.org/10.1111/j.1365-294X.2010.04934.x.
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.
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.
Koch P B, Behnecke B, Weigmann-Lenz M, Ffrench-Constant R H. 2000. Insect pigmentation:activities of β-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.
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)
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.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14):1 754-1 760, https://doi.org/10.1093/bioinformatics/btp324.
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):1 032-1 037, https://doi.org/10.16213/j.cnki.scjas.2016.05.008. (in Chinese with English abstract)
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)
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.
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.
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):3 787-3 793, https://doi.org/10.1093/bioinformatics/bti430.
Metzker M L. 2010. Sequencing technologies-the next generation. Nature Reviews Genetics, 11(1):31-46, https://doi.org/10.1038/nrg2626.
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.
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):1 499-1 503, https://doi.org/10.1016/S0006-2952(03)00504-5.
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.
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.
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):1 327-1 337, https://doi.org/10.1083/jcb.97.5.1327.
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.
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.
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.
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.
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.
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)
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)
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.
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.
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):1 474-1 480, https://doi.org/10.1111/j.1365-2109.2009.02247.x.
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.
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):38 159-38 165, https://doi.org/10.1074/jbc.M105454200.
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.
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)
Copyright © Haiyang Xuebao