Molecular and physiological adaptations to low-salinity stress in penaeid shrimp: a focus on Litopenaeus vannamei and Penaeus monodon

Abstract

Penaeid shrimp are economically important in global aquaculture. Rising demand has expanded shrimp farming and supported coastal economies. Low-salinity (hyposalinity) stress is a major constraint that impairs physiology and reduces growth, survival, and productivity. This review explores the adaptive mechanisms employed by penaeid shrimp in response to salinity stress and the consequent challenges faced by the aquaculture sector. Penaeid shrimp exhibit adaptive responses to salinity stress through a variety of physiological and molecular mechanisms, including ion regulation, osmoregulation, antioxidant defense, and the activation of signaling pathways. While these mechanisms are critical, they necessitate further in-depth investigation. This review synthesizes recent advancements in the understanding of penaeid shrimp adaptation to salinity stress, encompassing salinity signal perception, the activation of calcium and phospholipid signaling, signal transduction, and the regulation of gene expression. Additionally, it provides a comprehensive overview of the physiological and molecular responses of penaeid shrimp to salinity stress. The paper also discusses the potential implications of these findings for the aquaculture industry, particularly for improving climate-change resilience under increasingly frequent and unpredictable salinity fluctuations.

Keywords

Penaeid shrimp / Salinity stress / Molecular mechanism / Aquaculture / Signal transfer

References

[1] Aweya JJ, Zhuang K, Liu Y, Fan J, Yao D, Wang F, et al.. The ARM repeat domain of hemocyanin interacts with MKK4 to modulate antimicrobial peptides expression. iScience, 2022, 25 Article ID: 103958

[2] Blaustein MP, Lariccia V, Khananshvili D, Annunziato L, Verkhratsky A. Multipurpose Na(+) ions mediate excitation and cellular homeostasis: evolution of the concept of Na(+) pumps and Na(+)/Ca(2+) exchangers. Cell Calcium, 2020, 87 Article ID: 102166

[3] Burgoyne JR. Oxidative stress impairs autophagy through oxidation of ATG3 and ATG7. Autophagy, 2018, 14: 1092-1093

[4] Cao QH, Liu F, Yang ZL, Fu XH, Yang ZH, Liu Q, et al.. Prognostic value of autophagy related proteins ULK1, Beclin 1, ATG3, ATG5, ATG7, ATG9, ATG10, ATG12, LC3B and p62/SQSTM1 in gastric cancer. Am J Transl Res, 2016, 8: 3831-3847

[5] Chaichanit N, Wonglapsuwan M, Chotigeat W. Ribosomal protein L10A and signaling pathway. Gene, 2018, 674: 170-177

[6] Chen YH, Zhao L, Pang LR, Li XY, Weng SP, He JG. Identification and characterization of Inositol-requiring enzyme-1 and X-box binding protein 1, two proteins involved in the unfolded protein response of Litopenaeus vannamei. Dev Comp Immunol, 2012, 38: 66-77

[7] Chen S-J, Gao Y-J, Xie S-W, Niu J, Yang F, Fang W-P, et al.. Effect ofl-ascorbyl-2-polyphosphate supplementation on growth performance, body composition, antioxidative capacity and salinity stress tolerance of juvenile Pacific white shrimp, Litopenaeus vannamei. Aquac Res, 2017, 48: 4608-4622

[8] Chen SJ, Guo YC, Espe M, Yang F, Fang WP, Wan MG, et al.. Growth performance, haematological parameters, antioxidant status and salinity stress tolerance of juvenile Pacific white shrimp ( Litopenaeus vannamei ) fed different levels of dietary myo-inositol. Aquac Nutr, 2018, 24: 1527-1539

[9] Chen T, Ren C, Jiang X, Zhang L, Li H, Huang W, et al.. Mechanisms for type-II vitellogenesis-inhibiting hormone suppression of vitellogenin transcription in shrimp hepatopancreas: crosstalk of GC/cGMP pathway with different MAPK-dependent cascades. PLoS ONE, 2018, 13 Article ID: e0194459

[10] Chen S, Yu Y, Gao Y, Yin P, Tian L, Niu J, et al.. Exposure to acute ammonia stress influences survival, immune response and antioxidant status of pacific white shrimp ( Litopenaeus vannamei ) pretreated with diverse levels of inositol. Fish Shellfish Immunol, 2019, 89: 248-256

[11] Chen Y, Zhou L, Yu Q, Li E, Xie J. Effects of Sulfamethoxazole and Florfenicol on growth, antioxidant capacity, immune responses and intestinal microbiota in Pacific white shrimp Litopenaeus vannamei at low salinity. Antibiotics (Basel), 2023

[12] Cheng W, Chen JC. Effects of pH, temperature and salinity on immune parameters of the freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol, 2000, 10: 387-391

[13] Cheng KM, Hu CQ, Liu YN, Zheng SX, Qi XJ. Dietary magnesium requirement and physiological responses of marine shrimp Litopenaeus vannamei reared in low salinity water. Aquacult Nutr, 2005, 11: 385-393

[14] Cheng K-m, Hu C-q, Liu Y-n, Zheng S-x, Qi X-j. Effects of dietary calcium, phosphorus and calcium/phosphorus ratio on the growth and tissue mineralization of Litopenaeus vannamei reared in low-salinity water. Aquaculture, 2006, 251: 472-483

[15] Cheng AC, Lin CJ, Wang ST, Liu CH. Salinity stress impairs disease resistance in white shrimp, Penaeus vannamei through AMPK pathway, ameliorated by dietary glucose-mediated energy homeostasis. Comp Biochem Physiol A Mol Integr Physiol, 2025, 302 Article ID: 111799

[16] Chotphruethipong L, Chanvorachote P, Reudhabibadh R, Singh A, Benjakul S, Roytrakul S, Hutamekalin PChitooligosaccharide from Pacific White Shrimp Shell Chitosan Ameliorates Inflammation and Oxidative Stress via NF-κB, Erk1/2, Akt and Nrf2/HO-1 Pathways in LPS-Induced RAW264.7 Macrophage Cells2023Foods

[17] Deepika A, Sreedharan K, Paria A, Makesh M, Rajendran KV. Toll-pathway in tiger shrimp (Penaeus monodon) responds to white spot syndrome virus infection: evidence through molecular characterisation and expression profiles of MyD88, TRAF6 and TLR genes. Fish Shellfish Immunol, 2014, 41: 441-454

[18] Demaurex N, Poburko D, Frieden M. Regulation of plasma membrane calcium fluxes by mitochondria. Biochim Biophys Acta, 2009, 1787: 1383-1394

[19] Diao J, Liu R, Rong Y, Zhao M, Zhang J, Lai Y, et al.. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature, 2015, 520: 563-566

[20] Duan Y, Nan Y, Xiao M, Yang Y. Toxicity of three microcystin variants on the histology, physiological and metabolism of hepatopancreas and intestinal microbiota of Litopenaeus vannamei. Comp Biochem Physiol C Toxicol Pharmacol, 2024, 280 Article ID: 109904

[21] Fabri LM, Lucena MN, Garcon DP, Moraes CM, McNamara JC, Leone FA. Kinetic characterization of the gill (Na⁺, K⁺)-ATPase in a hololimnetic population of the diadromous Amazon River shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp Biochem Physiol B Biochem Mol Biol, 2019, 227: 64-74

[22] Fan H, Li Y, Yang Q, Jiang S, Yang L, Huang J, et al.. Isolation and characterization of a MAPKK gene from Penaeus monodon in response to bacterial infection and low-salinity challenge. Aquac Rep, 2021

[23] Feng W, Su S, Song C, Yu F, Zhou J, Li J, et al.. Effects of copper exposure on oxidative stress, apoptosis, endoplasmic reticulum stress, autophagy and immune response in different tissues of Chinese mitten crab ( Eriocheir sinensis ). Antioxidants, 2022

[24] Freire CA, Onken H, McNamara JC. A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A Mol Integr Physiol, 2008, 151: 272-304

[25] Fu L, Peng J, Zhao S, Zhang Y, Su X, Wang Y. Lactic acid bacteria-specific induction of CD4(+)Foxp3(+)T cells ameliorates shrimp tropomyosin-induced allergic response in mice via suppression of mTOR signaling. Sci Rep, 2017, 7 Article ID: 1987

[26] Gao W, Tian L, Huang T, Yao M, Hu W, Xu Q. Effect of salinity on the growth performance, osmolarity and metabolism-related gene expression in white shrimp Litopenaeus vannamei. Aquac Rep, 2016, 4: 125-129

[27] Gao J, Song YJ, Wang H, Zhao BR, Wang XW. Mindin activates autophagy for lipid utilization and facilitates White Spot Syndrome Virus infection in shrimp. Mbio, 2023, 14 Article ID: e0291922

[28] Garcon DP, Fabri LM, Moraes CM, Costa MIC, Freitas RS, McNamara JC, et al.. Effects of ammonia on gill (Na(+), K(+))-ATPase kinetics in a hololimnetic population of the Amazon River shrimp Macrobrachium amazonicum. Aquat Toxicol, 2022, 246 Article ID: 106144

[29] Giffard-Mena I, Ponce-Rivas E, Sigala-Andrade HM, Uranga-Solis C, Re AD, Diaz F, et al.. Evaluation of the osmoregulatory capacity and three stress biomarkers in white shrimp Penaeus vannamei exposed to different temperature and salinity conditions: Na(+)/K(+) ATPase, Heat Shock Proteins (HSP), and Crustacean Hyperglycemic Hormones (CHHs). Comp Biochem Physiol B Biochem Mol Biol, 2024, 271 Article ID: 110942

[30] Gu HJ, Sun QL, Jiang S, Zhang J, Sun L. First characterization of an anti-lipopolysaccharide factor (ALF) from hydrothermal vent shrimp: insights into the immune function of deep-sea crustacean ALF. Dev Comp Immunol, 2018, 84: 382-395

[31] He N, Qin Q, Xu X. Differential profile of genes expressed in hemocytes of White Spot Syndrome Virus-resistant shrimp (Penaeus japonicus) by combining suppression subtractive hybridization and differential hybridization. Antiviral Res, 2005, 66: 39-45

[32] He S, Qian Z, Yang J, Wang X, Mi X, Liu Y, et al.. Molecular characterization of a p38 MAPK from Litopenaeus vannamei and its expression during the molt cycle and following pathogen infection. Dev Comp Immunol, 2013, 41: 217-221

[33] He Y, Yao W, Liu P, Li J, Wang Q. Expression profiles of the p38 MAPK signaling pathway from Chinese shrimp Fenneropenaeus chinensis in response to viral and bacterial infections. Gene, 2018, 642: 381-388

[34] Hsieh YC, Chen YM, Li CY, Chang YH, Liang SY, Lin SY, et al.. To complete its replication cycle, a shrimp virus changes the population of long chain fatty acids during infection via the PI3K-Akt-mTOR-HIF1α pathway. Dev Comp Immunol, 2015, 53(1): 85-95

[35] Hu D, Pan L, Zhao Q, Ren Q. Transcriptomic response to low salinity stress in gills of the Pacific white shrimp, Litopenaeus vannamei. Mar Genomics, 2015, 24(3): 297-304

[36] Hu R, Dong W, Liang Q, Wang F, Ou M, Li Z, et al.. A Litopenaeus vannamei p70S6K gene is involved in the antioxidative and apoptosis under low temperature. Fish Shellfish Immunol, 2020, 106: 656-665

[37] Huang W, Ren C, Li H, Huo D, Wang Y, Jiang X, et al.. Transcriptomic analyses on muscle tissues of Litopenaeus vannamei provide the first profile insight into the response to low temperature stress. PLoS ONE, 2017, 12 Article ID: e0178604

[38] Huang H, Huang C, Guo L, Zeng C, Ye H. Profiles of calreticulin and Ca2+ concentration under low temperature and salinity stress in the mud crab, Scylla paramamosain. PLoS ONE, 2019, 14 Article ID: e0220405

[39] Huang M, Dong Y, Zhang Y, Chen Q, Xie J, Xu C, et al.. Growth and lipidomic responses of juvenile Pacific white shrimp Litopenaeus vannamei to low salinity. Front Physiol, 2019, 10 Article ID: 1087

[40] Huang Z, Zheng X, Chen Z, Zheng Z, Yao D, Yang S, et al.. Modulation of SREBP expression and fatty acid levels by bacteria-induced ER stress is mediated by hemocyanin in Penaeid shrimp. Mar Drugs, 2023

[41] Huang S, Jiang S, Jiang S, Huang J, Yang Q, Yang L, et al.. Omics analysis of Penaeus monodon in response to salinity changes. Stress Biology, 2025

[42] Jiang J, Jiang B, He Z, Ficarro SB, Che J, Marto JA, et al.. Discovery of covalent MKK4/7 dual inhibitor. Cell Chem Biol, 2020, 27: 1553-1560 e8

[43] K A, Sebastian SR, K SS, Nair A, M VA, Singh ISB, Philip R (2021) Molecular and Functional Characterization of an Anti-lipopolysaccharide Factor Mm-ALF from Speckled Shrimp Metapenaeus monoceros. Probiotics Antimicrob Proteins 2021; 13: 1183–1194.https://doi.org/10.1007/s12602-021-09741-3

[44] Kaiser SE, Qiu Y, Coats JE, Mao K, Klionsky DJ, Schulman BA. Structures of Atg7-Atg3 and Atg7-Atg10 reveal noncanonical mechanisms of E2 recruitment by the autophagy E1. Autophagy, 2013, 9: 778-780

[45] Kim DH, Lee YH, Sayed AEH, Choi IY, Lee JS. Genome-wide identification of 194 G protein-coupled receptor (GPCR) genes from the water flea Daphnia magna. Comp Biochem Physiol Part D Genomics Proteomics, 2022, 42 Article ID: 100983

[46] Kim DH, Park JC, Lee JS. G protein-coupled receptors (GPCRs) in rotifers and cladocerans: potential applications in ecotoxicology, ecophysiology, comparative endocrinology, and pharmacology. Comp Biochem Physiol C Toxicol Pharmacol, 2022, 256 Article ID: 109297

[47] Kruangkum T, Jaiboon K, Pakawanit P, Saetan J, Pudgerd A, Wannapaiboon S, et al.. Anatomical and molecular insights into the antennal gland of the giant freshwater prawn Macrobrachium rosenbergii. Cell Tissue Res, 2024, 397: 125-146

[48] Leone FA, Masui DC, de Souza Bezerra TM, Garcon DP, Valenti WC, Augusto AS, et al.. Kinetic analysis of gill (Na(+),K(+))-ATPase activity in selected ontogenetic stages of the Amazon River shrimp, Macrobrachium amazonicum (Decapoda, Palaemonidae): interactions at ATP- and cation-binding sites. J Membr Biol, 2012, 245: 201-215

[49] Leone FA, Bezerra TM, Garcon DP, Lucena MN, Pinto MR, Fontes CF, et al.. Modulation by K+ plus NH4+ of microsomal (Na+, K+)-ATPase activity in selected ontogenetic stages of the diadromous river shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). PLoS ONE, 2014, 9 Article ID: e89625

[50] Li X, Meng X, Kong J, Luo K, Luan S, Cao B, et al.. Identification, cloning and characterization of an extracellular signal-regulated kinase (ERK) from Chinese shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol, 2013, 35: 1882-1890

[51] Li E, Wang X, Chen K, Xu C, Qin JG, Chen L. Physiological change and nutritional requirement of Pacific white shrimp Litopenaeus vannamei at low salinity. Rev Aquacult, 2015, 9: 57-75

[52] Li S, Lv X, Li F, Xiang J. Characterization of a lymphoid organ specific anti-lipopolysaccharide factor from shrimp reveals structure-activity relationship of the LPS-binding domain. Front Immunol, 2019, 10 Article ID: 872

[53] Li YD, Si MR, Jiang SG, Yang QB, Jiang S, Yang LS, et al.. Transcriptome and molecular regulatory mechanisms analysis of gills in the black tiger shrimp Penaeus monodon under chronic low-salinity stress. Front Physiol, 2023, 14 Article ID: 1118341

[54] Li C, Zhang P, Hong PP, Niu GJ, Wang XP, Zhao XF, et al.. White spot syndrome virus hijacks host PP2A-FOXO axes to promote its propagation. Int J Biol Macromol, 2024, 256 Article ID: 128333

[55] Li Z, Chang T, Han F, Fan X, Liu W, Wu P, et al.. Effects of myo-inositol on growth and biomarkers of environmental stress and metabolic regulation in Pacific white shrimp ( Litopenaeus vannamei ) reared at low salinity. Comp Biochem Physiol D Genomics Proteomics, 2024, 50 Article ID: 101216

[56] Li Y, Gao P, Ye Y, Li Y, Sun Z, Li L, et al.. Transcriptome analysis reveals the key genes and pathways for growth, ion transport, and oxidative stress in post-larval black tiger shrimp ( Penaeus monodon ) under acute low salt stress. Mar Biotechnol (NY), 2025, 27 Article ID: 34

[57] Liu H, Zhang X, Tan B, Lin Y, Chi S, Dong X, et al.. Effect of dietary potassium on growth, nitrogen metabolism, osmoregulation and immunity of pacific white shrimp ( Litopenaeus vannamei ) reared in low salinity seawater. J Ocean Univ China, 2013, 13: 311-320

[58] Liu Y, Yu Y, Li S, Sun M, Li F. Comparative transcriptomic analysis of gill reveals genes belonging to mTORC1 signaling pathway associated with the resistance trait of shrimp to VP(AHPND). Front Immunol, 2023, 14 Article ID: 1150628

[59] Liu Q, Xu D, Jiang S, Huang J, Zhou F, Yang Q, Jiang S, Yang L (2018) Toll-receptor 9 gene in the black tiger shrimp (Penaeus monodon) induced the activation of the TLR-NF-kappaB signaling pathway. Gene 2018; 639: 27–33.https://doi.org/10.1016/j.gene.2017.09.060

[60] Long X, Wu X, Zhao L, Ye H, Cheng Y, Zeng C. Physiological responses and ovarian development of female Chinese mitten crab Eriocheir sinensis subjected to different salinity conditions. Front Physiol, 2017, 8 Article ID: 1072

[61] Luo K, Guo Z, Liu Y, Li C, Ma Z, Tian X. Responses of growth performance, immunity, disease resistance of shrimp and microbiota in Penaeus vannamei culture system to Bacillus subtilis BSXE-1601 administration: dietary supplementation versus water addition. Microbiol Res, 2024, 283 Article ID: 127693

[62] Luo Z, Yu Y, Zhang Q, Bao Z, Xiang J, Li F. Comparative Transcriptome Analysis Reveals the Adaptation Mechanism to High Salinity in Litopenaeus vannamei. Frontiers in Marine Science 2022; 9.https://doi.org/10.3389/fmars.2022.864338

[63] Mantovani M, McNamara JC. Contrasting strategies of osmotic and ionic regulation in freshwater crabs and shrimps: gene expression of gill ion transporters. J Exp Biol 2021; 224.https://doi.org/10.1242/jeb.233890

[64] Mendonca NN, Masui DC, McNamara JC, Leone FA, Furriel RP. Long-term exposure of the freshwater shrimp Macrobrachium olfersii to elevated salinity: Effects on gill (Na+,K+)-ATPase α-subunit expression and K+-phosphatase activity. Comp Biochem Physiol A Mol Integr Physiol, 2007, 146: 534-543

[65] Mo N, Shao S, Zhuang Y, Yang Y, Cui Z, Bao C. Activation and characterization of G protein-coupled receptors for CHHs in the mud crab, Scylla paramamosain. Comp Biochem Physiol A Mol Integr Physiol, 2024, 288 Article ID: 111563

[66] Mykles DL. Signaling pathways that regulate the crustacean molting gland. Front Endocrinol (Lausanne), 2021, 12 Article ID: 674711

[67] Noor HB, Mou NA, Salem L, Shimul MFA, Biswas S, Akther R, et al.. Anti-inflammatory property of AMP-activated protein kinase. Antiinflamm Antiallergy Agents Med Chem, 2020, 19: 2-41

[68] Ou J, Liu Q, Bian Y, Luan X, Meng Y, Dong H, et al.. Integrated analysis of mRNA and microRNA transcriptome related to immunity and autophagy in shrimp hemocytes infected with Spiroplasma eriocheiris. Fish Shellfish Immunol, 2022, 130: 436-452

[69] Pan L, Si L, Hu D. Ion transport signal pathways mediated by neurotransmitter (biogenic amines) of Litopenaeus vannamei under low salinity challenge. J Ocean Univ China, 2019, 18: 210-218

[70] Proietti Onori M, van Woerden GM. Role of calcium/calmodulin-dependent kinase 2 in neurodevelopmental disorders. Brain Res Bull, 2021, 171: 209-220

[71] Qiu W, He JH, Zuo H, Niu S, Li C, Zhang S, et al.. Identification, characterization, and function analysis of the NF-κB repressing factor (NKRF) gene from Litopenaeus vannamei. Dev Comp Immunol, 2017, 76: 83-92

[72] Rabanal-Ruiz Y, Otten EG, Korolchuk VI. Mtorc1 as the main gateway to autophagy. Essays Biochem, 2017, 61: 565-584

[73] Rahi ML, Azad KN, Tabassum M, Irin HH, Hossain KS, Aziz D, et al.. Effects of salinity on physiological, biochemical and gene expression parameters of black tiger shrimp ( Penaeus monodon ): potential for farming in low-salinity environments. Biology (Basel), 2021

[74] Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol, 2007, 8: 519-529

[75] Saez AG, Escalante R, Sastre L. High DNA sequence variability at the alpha 1 Na/K-ATPase locus of Artemia franciscana (brine shrimp): polymorphism in a gene for salt-resistance in a salt-resistant organism. Mol Biol Evol, 2000, 17: 235-250

[76] Sangklai N, Supungul P, Jaroenlak P, Tassanakajon A. Immune signaling of Litopenaeus vannamei c-type lysozyme and its role during microsporidian Enterocytozoon hepatopenaei (EHP) infection. PLoS Pathog, 2024, 20 Article ID: e1012199

[77] Sharif R, Ghazali AR, Rajab NF, Haron H, Osman F. Toxicological evaluation of some Malaysian locally processed raw food products. Food Chem Toxicol, 2008, 46: 368-374

[78] Shekhar MS, Kiruthika J, Rajesh S, Ponniah AG. High salinity induced expression profiling of differentially expressed genes in shrimp (Penaeus monodon). Mol Biol Rep, 2014, 41: 6275-6289

[79] Su MA, Huang YT, Chen IT, Lee DY, Hsieh YC, Li CY, et al.. An invertebrate Warburg effect: a shrimp virus achieves successful replication by altering the host metabolome via the PI3K-Akt-mTOR pathway. PLoS Pathog, 2014, 10 Article ID: e1004196

[80] Sun S, Zhu M, Pan F, Feng J, Li J. Identifying neuropeptide and G protein-coupled receptors of juvenile Oriental River prawn (Macrobrachium nipponense) in response to salinity acclimation. Front Endocrinol (Lausanne), 2020, 11 Article ID: 623

[81] Uengwetwanit T, Pootakham W, Nookaew I, Sonthirod C, Angthong P, Sittikankaew K, et al.. A chromosome-level assembly of the black tiger shrimp ( Penaeus monodon ) genome facilitates the identification of growth-associated genes. Mol Ecol Resour, 2021, 21: 1620-1640

[82] Viet Nguyen T, Ryan LW, Nocillado J, Le Groumellec M, Elizur A, Ventura T. Transcriptomic changes across vitellogenesis in the black tiger prawn (Penaeus monodon), neuropeptides and G protein-coupled receptors repertoire curation. Gen Comp Endocrinol, 2020, 298 Article ID: 113585

[83] Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science, 2011, 334: 1081-1086

[84] Wang LU, Chen JC. The immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus at different salinity levels. Fish Shellfish Immunol, 2005, 18: 269-278

[85] Wang JQ, Hou L, Yi N, Zhang RF, Zou XY. Molecular analysis and its expression of a pou homeobox protein gene during development and in response to salinity stress from brine shrimp, Artemia sinica. Comp Biochem Physiol A Mol Integr Physiol, 2012, 161: 36-43

[86] Wang PH, Wan DH, Gu ZH, Qiu W, Chen YG, Weng SP, et al.. Analysis of expression, cellular localization, and function of three inhibitors of apoptosis (IAPs) from Litopenaeus vannamei during WSSV infection and in regulation of antimicrobial peptide genes (AMPs). PLoS ONE, 2013, 8 Article ID: e72592

[87] Wang Y, Duan Y, Huang J, Wang J, Zhou C, Jiang S, et al.. Characterization and functional study of nuclear factor erythroid 2-related factor 2 (Nrf2) in black tiger shrimp ( Penaeus monodon ). Fish Shellfish Immunol, 2021, 119: 289-299

[88] Wang C, Zhang Z, Deng Z, Sun J, Zhao R, Cui Y, et al.. Classical aquaporins from Pacific white shrimp ( Litopenaeus vannamei ): molecular characterization and expression analysis in hypersalinity. Aquac Rep, 2022

[89] Wang S, Li H, Chen R, Jiang X, He J, Li C. TAK1 confers antibacterial protection through mediating the activation of MAPK and NF-κB pathways in shrimp. Fish Shellfish Immunol, 2022, 123: 248-256

[90] Wei Y, Xu H, Zhou Z, Wang P, Cheng W, Huang H, et al.. Chromosome-level genome assembly and annotation of the kuruma shrimp Marsupenaeus japonicus. Sci Data, 2025, 12 Article ID: 2028

[91] Xiao F, Wang J, Liu H, Zhuang M, Wen X, Zhao H, et al.. Effects of dietary protein levels on growth, digestive enzyme activity, antioxidant capacity, and gene expression related to muscle growth and protein synthesis of juvenile greasyback shrimp ( Metapenaeus ensis ). Animals, 2023

[92] Xu C, Li E, Xu Z, Wang S, Chen K, Wang X, et al.. Molecular characterization and expression of AMP-activated protein kinase in response to low-salinity stress in the Pacific white shrimp Litopenaeus vannamei. Comp Biochem Physiol B Biochem Mol Biol, 2016, 198: 79-90

[93] Yan L, Su J, Wang Z, Yan X, Yu R, Ma P, et al.. Transcriptomic analysis of Crassostrea sikamea × Crassostrea angulata hybrids in response to low salinity stress. PLoS ONE, 2017, 12 Article ID: e0171483

[94] Yang L, Luo M, Guo Z, Zuo H, Weng S, He J, et al.. A shrimp gene encoding a single WAP domain (SWD)-containing protein regulated by JAK-STAT and NF-κB pathways. Dev Comp Immunol, 2020, 104 Article ID: 103537

[95] Ye Y, Ma J, Du X, Huang J, Zhou Y, Liu H, et al.. Integrated transcriptomic and metabolomic analyses reveal the adaptive mechanisms of a low-salinity selected population of Pacific white shrimp ( Litopenaeus vannamei ). Mar Biotechnol, 2025, 27: 154

[96] Yin X, Zhuang X, Luo W, Liao M, Huang L, Cui Q, et al.. Andrographolide promote the growth and immunity of Litopenaeus vannamei , and protects shrimps against Vibrio alginolyticus by regulating inflammation and apoptosis via a ROS-JNK dependent pathway. Front Immunol, 2022, 13 Article ID: 990297

[97] Yu Q, Han F, Rombenso A, Qin JG, Chen L, Li E. Dietary selenium supplementation alleviates low salinity stress in the Pacific white shrimp Litopenaeus vannamei: growth, antioxidative capacity and hepatopancreas transcriptomic responses. Br J Nutr 2023; 130: 933–943.https://doi.org/10.1017/S0007114522004032

[98] Yuan J, Zhang X, Liu C, Yu Y, Wei J, Li F, et al.. Genomic resources and comparative analyses of two economical penaeid shrimp species, Marsupenaeus japonicus and Penaeus monodon. Mar Genomics, 2018, 39: 22-25

[99] Zhai X, Yuan S, Yang X, Zou P, Li L, Li G, et al.. Chitosan oligosaccharides induce apoptosis in human renal carcinoma via reactive-oxygen-species-dependent endoplasmic reticulum stress. J Agric Food Chem, 2019, 67: 1691-1701

[100] Zhang X, Yuan J, Sun Y, Li S, Gao Y, Yu Y, et al.. Penaeid shrimp genome provides insights into benthic adaptation and frequent molting. Nat Commun, 2019, 10 Article ID: 356

[101] Zhao Q, Pan L, Ren Q, Wang L, Miao J. Effect of salinity on regulation mechanism of neuroendocrine-immunoregulatory network in Litopenaeus vannamei. Fish Shellfish Immunol, 2016, 49: 396-406

[102] Zhao C, Peng C, Wang P, Yan L, Fan S, Qiu L. Identification of a shrimp E3 ubiquitin ligase TRIM50-like involved in restricting white spot syndrome virus proliferation by its mediated autophagy and ubiquitination. Front Immunol, 2021, 12 Article ID: 682562

[103] Zhao W, Luo H, Zhu W, Yuan X, Shao J. Effects of time-dependent protein restriction on growth performance, digestibility, and mTOR signaling pathways in juvenile white shrimp Litopenaeus vannamei. Front Physiol, 2021, 12 Article ID: 661107

Funding

National Key R & D Program of China (2022YFD2401900)

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