Abstract
High-pH tolerance and growth are important traits for the shrimp culture industry in areas with saline-alkali water. In the present study, an F1 full-sib family of Pacific white shrimp (Litopenaeus vannamei) was generated with a new “semidirectional cross” method, and double-digest restriction site-associated DNA sequencing (ddRAD-Seq) technology was applied to genotype the 2 parents and 148 progenies. A total of 3567 high-quality markers were constructed for the genetic linkage map, and the total map length was 4161.555 centimorgans (cM), showing 48 linkage groups (LGs) with an average interlocus length of 1.167 cM. With a constrained logarithm of odds (LOD) score ≥ 2.50, 12 high-pH tolerance and 2 growth (body weight) QTLs were located. L. vannamei genomic scaffolds were used to assist with the detection of 21 stress- and 5 growth-related scaffold genes. According to the high-pH transcriptome data of our previous study, 6 candidate high-pH response genes were discovered, and 5 of these 6 genes were consistently expressed with the high-pH transcriptome data, validating the locations of the high-pH tolerance trait-related QTLs in this study. This paper is the first report of fine-mapping high-pH tolerance and growth (body weight) trait QTLs in one L. vannamei genetic map. Our results will further benefit marker-assisted selection work and might be useful for promoting genomic research on the shrimp L. vannamei.
Similar content being viewed by others
References
Abdelrahman ElHady M, Alcivar-Warren A, Allen S, Al-Tobasei R, Bao L, Beck B, Blackburn H, Bosworth B, Buchanan J, Chappell J, Daniels W, Dong S, Dunham R, Durland E, Elaswad A, Gomez-Chiarri M, Gosh K, Guo X, Hackett P, Hanson T, Hedgecock D, Howard T, Holland L, Jackson M, Jin Y, Khalil K, Kocher T, Leeds T, Li N, Lindsey L, Liu S, Liu Z, Martin K, Novriadi R, Odin R, Palti Y, Peatman E, Proestou D, Qin G, Reading B, Rexroad C, Roberts S, Salem M, Severin A, Shi H, Shoemaker C, Stiles S, Tan S, Tang KF, Thongda W, Tiersch T, Tomasso J, Prabowo WT, Vallejo R, van der Steen H, Vo K, Waldbieser G, Wang H, Wang X, Xiang J, Yang Y, Yant R, Yuan Z, Zeng Q, Zhou T (2017) Aquaculture genomics, genetics and breeding in the United States: current status, challenges, and priorities for future research. BMC Genomics 18:191
Adelman K, Marr MT, Werner J, Saunders A, Ni Z, Andrulis ED, Lis JT (2005) Efficient release from promoter-proximal stall sites requires transcript cleavage factor TFIIS. Mol Cell 17:103–112
Alcivar-Warren A, Meehan-Meola D, Park SW, Xu Z, Delaney M, Zuniga G (2007) ShrimpMap: a low-density, microsatellite-based linkage map of the pacific whiteleg shrimp, Litopenaeus vannamei: identification of sex-linked markers in linkage group. J Shellfish Res 26:1259–1277
Andriantahina F, Liu XL, Huang H (2013) Genetic map construction and quantitative trait locus (QTL) detection of growth-related traits in Litopenaeus vannamei for selective breeding applications. PLoS One 8:e75206
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376
Berthier-Schaad Y, Kao WH, Coresh J, Zhang L, Ingersoll RG, Stephens R, Smith MW (2007) Reliability of high-throughput genotyping of whole genome amplified DNA in SNP genotyping studies. Electrophoresis 28:2812–2817
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bourgeois YX, Lhuillier E, Cézard T, Bertrand JA, Delahaie B, Cornuault J, Duval T, Bouchez O, Milá B, Thébaud C (2013) Mass production of SNP markers in a nonmodel passerine bird through RAD sequencing and contig mapping to the zebra finch genome. Mol Ecol Resour 13:899–907
Blagoev B, Ong SE, Kratchmarova I, Mann M (2004) Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat Biotechnol 22:1139–1145
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140
Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR 3rd, Hays L, Morgan WF, Petrini JH (1998) The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477–486
Choi SH, Chung AR, Kang W, Park JY, Lee MS, Hwang SW, Kim DY, Kim SU, Ahn SH, Kim S, Han KH (2014) Silencing of hypoxia-inducible factor-1β induces anti-tumor effects in hepatoma cell lines under tumor hypoxia. PLoS One 9:e103304
Chuang SM, Madura K (2005) Saccharomyces cerevisiae Ub-conjugating enzyme Ubc4 binds the proteasome in the presence of translationally damaged proteins. Genetics 171:1477–1484
Cross TG, Scheel-Toellner D, Henriquez NV, Deacon E, Salmon M, Lord JM (2000) Serine/threonine protein kinases and apoptosis. Exp Cell Res 256:34–41
Dai X, Wang T, Gonzalez G, Wang Y (2018) Identification of YTH domain-containing proteins as the readers for N1-methyladenosine in RNA. Anal Chem 90:6380–6384
Das S, Upadhyaya HD, Bajaj D, Kujur A, Badoni S, Laxmi KV, Tripathi S, Gowda CL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Deploying QTL-seq for rapid delineation of a potential candidate gene underlying major trait-associated QTL in chickpea. DNA Res 22:193–203
de Vries MS, Webb SJ, Tu J, Cory E, Morgan V, Sah RL, Deheyn DD, Taylor JR (2016) Stress physiology and weapon integrity of intertidal mantis shrimp under future ocean conditions. Sci Rep 6:38637
Deng CX, Brodie SG (2000) Roles of BRCA1 and its interacting proteins. Bioessays 22:728–737
Du ZQ, Ciobanu DC, Onteru SK, Gorbach D, Mileham AJ, Jaramillo G, Rothschild MF (2010) A gene-based SNP linkage map for pacific white shrimp, Litopenaeus vannamei. Anim Genet 41:286–294
FAO (2012) Fisheries and Aquaculture Department: the state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations, Rome, Italy, p 37
Fehsenfeld S, Kiko R, Appelhans Y, Towle D, Zimmer M, Melzner F (2011) Effects of elevated seawater pCO2 on gene expression patterns in the gills of the green crab, Carcinus maenas. BMC Genomics 12:488
Fu B, Liu H, Yu X, Tong J (2016) A high-density genetic map and growth related QTL mapping in bighead carp (Hypophthalmichthys nobilis). Sci Rep 6:28679
Geng X, Liu S, Yao J, Bao L, Zhang J, Li C, Wang R, Sha J, Zeng P, Zhi D, Liu Z (2016) A genome-wide association study identifies multiple regions associated with head size in catfish. G3 (Bethesda) 6:3389–3398
Goto Y, Hattori A, Ishii Y, Mizutani S, Tsujimoto M (2006) Enzymatic properties of human aminopeptidase a. regulation of its enzymatic activity by calcium and angiotensin IV. J Biol Chem 281:23503–23513
Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev AF, Tanaka K, Nakatani Y (2003) The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113:357–367
Horne I, Haritos VS, Oakeshott JG (2009) Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol 39:547–567
Huang W, Ren C, Li H, Huo D, Wang Y, Jiang X, Tian Y, Luo P, Chen T, Hu C (2017) Transcriptomic analyses on muscle tissues of Litopenaeus vannamei provide the first profile insight into the response to low temperature stress. PLoS One 12:e0178604
Huang W, Li H, Cheng C, Ren C, Chen T, Jiang X, Cheng K, Luo P, Hu C (2018) Analysis of the transcriptome data in Litopenaeus vannamei reveals the immune basis and predicts the hub regulation-genes in response to high-pH stress. PLoS One 13:e0207771
Ichikawa Y, Bayeva M, Ghanefar M, Potini V, Sun L, Mutharasan RK, Wu R, Khechaduri A, Jairaj Naik T, Ardehali H (2012) Disruption of ATP-binding cassette B8 in mice leads to cardiomyopathy through a decrease in mitochondrial iron export. Proc Natl Acad Sci U S A 109:4152–4157
Imprialou M, Petretto E, Bottolo L (2017) Expression QTLs mapping and analysis: a Bayesian perspective. Methods Mol Biol 1488:189–215
Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455
Kang HS, Beak JY, Kim YS, Petrovich RM, Collins JB, Grissom SF, Jetten AM (2006) NABP1, a novel RORgamma-regulated gene encoding a single-stranded nucleic-acid-binding protein. Biochem J 397:89–99
Kong S, Ke Q, Chen L, Zhou Z, Pu F, Zhao J, Bai H, Peng W, Xu P (2019) Constructing a high-density genetic linkage map for large yellow croaker (Larimichthys crocea) and mapping resistance trait against ciliate parasite Cryptocaryon irritans. Mar Biotechnol 21:262–275
Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CL (2015) Ultra-high density intraspecific genetic linkage maps accelerate identification of functionally relevant molecular tags governing important agronomic traits in chickpea. Sci Rep 5:9468
Li C, Chen J (2008) The immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus under low and high pH stress. Fish Shellfish Immun 25:701–709
Li E, Chen L, Zeng C, Chen X, Yu N, Lai Q, Qin JG (2007) Growth, body composition, respiration and ambient ammonia nitrogen tolerance of the juvenile white shrimp, Litopenaeus vannamei, at different salinities. Aquaculture 265:385–390
Li J, Pu L, Han M, Zhu M, Zhang R, Xiang Y (2014) Soil salinization research in China: advances and prospects. J Geogr Sci 24:943–960
Li HL, Gu XH, Li BJ, Chen CH, Lin HR, Xia JH (2017) Genome-wide QTL analysis identified significant associations between hypoxia tolerance and mutations in the GPR132 and ABCG4 genes in Nile Tilapia. Mar Biotechnol 19:441–453
Li BJ, Zhu ZX, Gu XH, Lin HR, Xia JH (2019) QTL mapping for red blotches in Malaysia red tilapia (Oreochromis spp.). Mar Biotechnol 21:384–395
Liang L, Ren B, Chang Y, Tang R, Zhang L (2013) Inland brackish (saline-alkaline) water resources and fisheries utilization in China. Chin Fish Econ 31:138–145 (In China)
Lien S, Gidskehaug L, Moen T, Hayes BJ, Berg PR, Davidson WS, Omholt SW, Kent MP (2011) A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics 12:615
Lin X, Taguchi A, Park S, Kushner JA, Li F, Li Y, White MF (2004) Dysregulation of insulin receptor substrate 2 in beta cells and brain causes obesity and diabetes. J Clin Invest 114:908–916
Linley AJ, Mathieu MG, Miles AK, Rees RC, McArdle SE, Regad T (2012) The helicase HAGE expressed by malignant melanoma-initiating cells is required for tumor cell proliferation in vivo. J Biol Chem 287:13633–13643
Liu C, Wang J, Zhang Y, Liu L (2008) Effects of salinity and Na+/K+ in percolating water from saline-alkali soil on the growth of Litopenaeus vannamei. Chin J Appl Ecol 19:1337–1342 (In China)
Liu Y, Fang H, Lai Q, Liang L (2016) The current state and development strategy for China’s saline-alkaline fisheries. Eng Sci CAE 18:74–78 (In China)
Liu H, Fu B, Me P, Feng X, Yu X, Tong J (2017) A high-density genetic linkage map and QTL fine mapping for body weight in crucian carp (Carassius auratus) using 2b-rad sequencing. G3 (Bethesda) 7:2473–2487
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Louro B, Kuh H, Tine M, de Koning DJ, Batargias C, Volckaert FAM, Reinhardt R, Canario AVM, Deborah M (2016) Power characterization and refinement of growth related quantitative trait loci in European sea bass (Dicentrarchus labrax) using a comparative approach. Aquaculture 455:8–21
Lu X, Luan S, Hu LY, Mao Y, Tao Y, Zhong SP, Kong J (2016) High-resolution genetic linkage mapping, high-temperature tolerance and growth-related quantitative trait locus (QTL) identification in Marsupenaeus japonicas. Mol Gen Genomics 291:1391–1405
Luan Z, Pan L, Dong S (2003) A study of the culture technology of shrimp in low-lying soline-alkali soil along the yellow river. Chin J Oceanol Limn 3:71–77 (In China)
MacFarlane AW 4th, Yamazaki T, Fang M, Sigal LJ, Kurosaki T, Campbell KS (2008) Enhanced NK-cell development and function in BCAP-deficient mice. Blood 112:131–140
Malkowska M, Kokoszynska K, Rychlewski L, Wyrwicz L (2013) Structural bioinformatics of the general transcription factor TFIID. Biochimie 95:680–691
Márquez J, Olaso E (2014) Role of discoidin domain receptor 2 in wound healing. Histol Histopathol 29:1355–1364
Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated. DNA (RAD) Markers 17:240–248
Ouellette LA, Reid RW, Blanchard SG, Brouwer CR (2018) LinkageMapView—rendering high-resolution linkage and QTL maps. Bioinformatics 34:306–307
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135
Piepho HP (2001) A quick method for computing approximate thresholds for quantitative trait loci detection. Genetics 157:425–432
Roggatz C, Lorch M, Hardege J, Benoit D (2016) Ocean acidification affects marine chemical communication by changing structure and function of peptide signaling molecules. Glob Change Biol 22:3914–3926
Rowe HC, Renaut S, Guggisberg A (2011) RAD in the realm of next generation sequencing technologies. Mol Ecol 20:3499–3502
Seo M, Peeters AJ, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JA, Koornneef M, Kamiya Y, Koshiba T (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci U S A 97:12908–12913
Separovic D, Hanada K, Maitah MY, Nagy B, Hang I, Tainsky MA, Kraniak JM, Bielawski J (2007) Sphingomyelin synthase 1 suppresses ceramide production and apoptosis post-photodamage. Biochem Biophys Res Commun 358:196–202
Shao C, Niu Y, Rastas P, Liu Y, Xie Z, Li H, Wang L, Jiang Y, Tai S, Tian Y, Sakamoto T, Chen S (2015) Genome-wide SNP identification for the construction of a high-resolution genetic map of Japanese flounder (Paralichthys olivaceus): applications to QTL mapping of Vibrio anguillarum disease resistance and comparative genomic analysis. DNA Res 22:161–170
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744
Stölting KN, Nipper R, Lindtke D, Caseys C, Waeber S, Castiglione S, Lexer C (2013) Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species. Mol Ecol 22:842–855
Soñanez-Organis JG, Peregrino-Uriarte AB, Gómez-Jiménez S, López-Zavala A, Forman HJ, Yepiz-Plascencia G (2009) Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissuespecific expression under hypoxia. Comp Biochem Physiol C Toxicol Pharmacol 150:395–405
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H (2013) SLAF-seq: an efficient method of large-scale denovo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8:e58700
Sun C, Niu Y, Ye X, Dong J, Hu W, Zeng Q, Chen Z, Tian Y, Zhang J, Lu M (2017) Construction of a high-density linkage map and mapping of sex determination and growth-related loci in the mandarin fish (Siniperca chuatsi). BMC Genomics 18:446
Tong JG, Sun XW (2015) Genetic and genomic analyses for economically important traits and their applications in molecular breeding of cultured fish. Science China-Life Sci 58:178–186
Toulany M, Rodemann HP (2015) Phosphatidylinositol 3-kinase/Akt signaling as a key mediator of tumor cell responsiveness to radiation. Semin Cancer Biol 35:180–190
van Daal A, Elgin SC (1992) A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell 3:593–602
Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an out breeding species. Genet Res 93:343–349
van Wijk SJ, Timmers HT (2010) The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J 24:981–993.
Wan SM, Liu H, Zhao BW, Nie CH, Wang WM, Gao ZX (2017) Construction of a high-density linkage map and fine mapping of QTLs for growth and gonad related traits in blunt snout bream. Sci Rep 7:46509
Wang PY, Weng J, Anderson RG (2005) OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation. Science 307:1472–1476
Wang WN, Zhou J, Wang P, Tian TT, Zheng Y, Liu Y, Mai WJ, Wang AL (2009) Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress. Comp Biochem Phys C 150:428–435
Wang S, Meyer E, McKay JK, Matz MV (2012) 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat Methods 9:808–810
Wang J, Luo MC, Chen Z, You FM, Wei Y, Zheng Y, Dvorak J (2013a) Aegilops tauschii single nucleotide polymorphisms shed light on the origins of wheat genome genetic diversity and pinpoint the geographic origin of hexaploid wheat. New Phytol 198:925–937
Wang X, Li E, Xiong Z, Chen K, Yu N, Du Z, Chen L (2013b) Low salinity decreases the tolerance to two pesticides, beta-cypermethrin and acephate, of whiteleg shrimp, Litopenaeus vannamei. J Aquac Res Development 4:190
Wang S, Feng Q, Zhou Y, Mao X, Chen Y, Xu H (2017) Dynamic changes in water and salinity in saline-alkali soils after simulated irrigation and leaching. PLoS One 12:e0187536
Wang X, Fu B, Yu X, Qu C, Zhang Q, Tong J (2018) Fine mapping of growth-related quantitative trait loci in Yellow River carp (Cyprinus carpio haematoperus). Aquaculture 484:277–285
Watt MJ, Spriet LL (2010) Triacylglycerol lipases and metabolic control: implications for health and disease. Am J Physiol Endocrinol Metab 299:E162–E168
Wu F, Wang T, Cui S, Xie Z, Dupont S, Zeng J, Gu H, Kong H, Hu M, Lu W, Wang Y (2017) Effects of seawater pH and temperature on foraging behavior of the Japanese stone crab Charybdis japonica. Mar Pollut Bull 120:99–108
Xu J, Zhao Z, Zhang X, Zheng X, Li J, Jiang Y, Kuang Y, Zhang Y, Feng J, Li C, Yu J, Li Q, Zhu Y, Liu Y, Xu P, Sun X (2014) Development and evaluation of the first high-throughput SNP array for common carp (Cyprinus carpio). BMC Genomics 15:307
Xue M (2018) Experiment and analysis of pond ecological farming technique in salt and alkaline soil of the yellow river beach. Shaanxi Water Resources 1:88–96 (In China)
Yu Y, Zhang X, Yuan J, Li F, Chen X, Zhao Y, Huang L, Zheng H, Xiang J (2015) Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific White Shrimp Litopenaeus vannamei. Sci Rep 5:15612
Yu Y, Wang Q, Zhang Q, Luo Z, Wang Y, Zhang X, Huang H, Xiang J, Li F (2019) Genome scan for genomic regions and genes associated with growth trait in pacific white shrimp Litopeneaus vannamei. Mar Biotechnol 21:374–383
Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396
Zhang D (2016) Technology for healthily breeding Penaeus vannamei boone in saline-alkali land of our country’s northern region. Shanxi Hydrotechnics 4:127–128 (In China)
Zhang G, Zhang X, Ye H, Jiang S, Yu H, Li J, Shi Q, Chen G, Zhou Z, Luo J, You X (2018) Construction of high-density genetic linkage maps and QTL mapping in the golden pompano. Aquaculture 482:90–95
Zhang X, Yuan J, Sun Y, Li S, Gao Y, Yu Y, Liu C, Wang Q, Lv X, Zhang X, Ma KY, Wang X, Lin W, Wang L, Zhu X, Zhang C, Zhang J, Jin S, Yu K, Kong J, Xu P, Chen J, Zhang H, Sorgeloos P, Sagi A, Alcivar-Warren A, Liu Z, Wang L, Ruan J, Chu KH, Liu B, Li F, Xiang J (2019) Penaeid shrimp genome provides insights into benthic adaptation and frequent molting. Nat Commun 10:356
Zimmerman SW, Yi YJ, Sutovsky M, van Leeuwen FW, Conant G, Sutovsky P (2014) Identification and characterization of RING-finger ubiquitin ligase UBR7 in mammalian spermatozoa. Cell Tissue Res 356:261–278
Acknowledgments
We thank the anonymous reviewers for comments on the manuscript.
Funding
This work was supported by the National Natural Science Foundation of China (No. 31602135), Institution of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences (No. ISEE2018PY03), the Science & Technology Promoting Projects for Oceanic & Fishery in Guangdong Province (SDYY-2018-01), and the Guangdong Province Program (2017B030314052, 2018A030313857, 2016A030310112, 2015A030310120, 2015B020231007 and A2015230).
Author information
Authors and Affiliations
Contributions
WH and CH contributed to project conception. Experiment and data analysis was conducted by WH, CC, JL, XZ, CR, XJ, TC, KC, and HL. The manuscript was prepared by WH. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Statement of Human and Animal Rights
Shrimp care and experiments were carried out according to the Care and Use of Agricultural Animals in Agricultural Research and Teaching and approved by the Science and Technology Bureau of China. Approval from the Department of Wildlife Administration was not required for the experiments conducted in this paper. All experiments in this paper were performed with permits obtained from the Government of the People’s Republic of China and endorsed by the Animal Experimentation Ethics Committee of Chinese Academy of Sciences.
Conflict of Interest
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Supplementary Table 1
(XLSX 12 kb)
Supplementary Table 2
(XLSX 9 kb)
Supplementary Table 3
(XLSX 9 kb)
Supplementary Table 4
(XLSX 777 kb)
Supplementary Table 5
(XLSX 775 kb)
Supplementary Fig. 1
Propagation characteristics of the shrimp L. vannamei. a Fertile female Pacific white shrimp, with a surgically removed eyestalk, which was usually used for stimulus-induced maturation of the shrimp, in the box, with arrows indicating the mature gonad of the female shrimp. b Fertile male Pacific white shrimp, with the spermatophore position of the male shrimp while packed with white spermatia shown in the framed area. c The thelycum position of the female shrimp, indicated by the arrow, with white spermatia adhering to the thelycum of the mated female shrimp. d The spermatophore position is framed, and the mated male parent is empty (without packed spermatium) in this position. Bars = 1 cm. (PDF 148 kb)
Rights and permissions
About this article
Cite this article
Huang, W., Cheng, C., Liu, J. et al. Fine Mapping of the High-pH Tolerance and Growth Trait-Related Quantitative Trait Loci (QTLs) and Identification of the Candidate Genes in Pacific White Shrimp (Litopenaeus vannamei). Mar Biotechnol 22, 1–18 (2020). https://doi.org/10.1007/s10126-019-09932-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-019-09932-8