Abstract
Giant freshwater prawn, Macrobrachium rosenbergii, is one of the major cultivated crustacean species in China. In recent years, a slow growth syndrome (SGS) has severely influenced the production, and the exact cause has not been clearly determined. In the present study, normal and SGS prawns were collected in 2016, 2017, and 2020. One-way ANOVA analysis showed significant difference in all growth traits examined between normal and SGS groups (P < 0.05). Cathepsin L (CatL) DNA fragment was cloned and re-sequenced, leading to identification of 41 SNPs. Among these SNPs and another four SNPs located in crustacean hyperglycemic hormone (CHH) that showed association with M. rosenbergii growth in Vietnam populations, 24 SNPs including two from the CHH gene were selected for association analysis. Eight out of the 24 SNPs were polymorphic in our population, in which SNP CatL-322 showed significant association with SGS (FDR adjusted P < 0.05). Fisher’s exact test was further conducted, and two intronic SNPs, CatL-322 and CHH-2409, showed significant association with carapace length of M. rosenbergii, explaining about 15 % of phenotypic variation in total. The two SNPs were further screened in a second population, and solid evidence was obtained. We compared the growth of different genotypes at each locus and confirmed that T allele at CatL-322 locus and G allele at CHH-2409 locus were beneficial to growth performance (P < 0.05). These two SNPs potentially can be applied in marker assisted selection in future M. rosenbergii breeding programs.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11756-021-00860-4/MediaObjects/11756_2021_860_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11756-021-00860-4/MediaObjects/11756_2021_860_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11756-021-00860-4/MediaObjects/11756_2021_860_Fig3_HTML.png)
Abbreviations
- SGS:
-
slow growth syndrome
- CatL:
-
cathepsin L
- CHH:
-
crustacean hyperglycemic hormone
- MIH:
-
molt-inhibiting hormone
- SNP:
-
single nucleotide polymorphism
- PCR:
-
polymerase chain reaction
- gDNA:
-
genomic DNA
- HWE:
-
Hardy-Weinberg Equilibrium
- FDR:
-
false discovery rate
References
Arockiaraj J et al (2013) Macrobrachium rosenbergii cathepsin L: Molecular characterization and gene expression in response to viral and bacterial infections. Microbiol Res 168(9):569–579. https://doi.org/10.1016/j.micres.2013.04.007
Chan S-M et al (1990) Effects of 20-hydroxyecdysone injection and eyestalk ablation on the moulting cycle of the shrimp, Penaeus vannamei. Comp Biochem Physiol A Physiol 96(1):205–209. https://doi.org/10.1016/0300-9629(90)90066-2
Chang ES (1985) Hormonal control of molting in decapod crustacea. Integr Comp Biol 25(1):179–185
Chang ES, Mykles DL (2011) Regulation of crustacean molting: a review and our perspectives. Gen Comp Endocrinol 172(3):323–330. https://doi.org/10.1016/j.ygcen.2011.04.003
de Almeida Marques HL, Moraes-Valenti PMC (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii (De Man 1879) and the Amazon river prawn Macrobrachium amazonicum (Heller 1862)) in Brazil. Aquac Res 43(7):984–992. https://doi.org/10.1111/j.1365-2109.2011.03032.x
Duan Y et al (2013) Cloning and expression analysis of Cathepsin L cDNA of Exopalaemon carinicauda. Zool Res 34(1):39–46. https://doi.org/10.3724/sp.j.1141.2013.01039
Easwvaran SP et al (2019) Enhanced muscle regeneration in freshwater prawn Macrobrachium rosenbergii achieved through in vivo silencing of the myostatin gene. J World Aquac Soc 50(5):1026–1039. https://doi.org/10.1111/jwas.12607
Fanjul-Moles ML (2006) Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update. Comp Biochem Physiol C: Toxicol Pharmacol 142(3–4):390–400. https://doi.org/10.1016/j.cbpc.2005.11.021
FAO (2019) FAO yearbook. Fishery and Aquaculture Statistics 2017/FAO annuaire. Statistiques des pêches et de l’aquaculture 2017/ FAO anuario. Estadísticas de pesca y acuicultura 2017. Rome/Roma
Fu H et al (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii) and the oriental river prawn (Macrobrachium nipponense) China. Aquac Res 43(7):993–998. https://doi.org/10.1111/j.1365-2109.2011.03085.x
Gabriel S et al (2009) SNP genoty** using the sequenom MassARRAY iPLEX Platform. Curr Protoc Hum Genet 60(1):2.12.11–12.12.18. https://doi.org/10.1002/0471142905.hg0212s60
Ganal MW et al (2009) SNP identification in crop plants. Curr Opin Plant Biol 12(2):211–217. https://doi.org/10.1016/j.pbi.2008.12.009
Glenn KL et al (2005) SNP analysis of AMY2 and CTSL genes in Litopenaeus vannamei and Penaeus monodon shrimp. Anim Genet 36(3):235–236. https://doi.org/10.1111/j.1365-2052.2005.01274.x
Haldar C et al (2019) "Single-nucleotide polymorphisms linked to body weight revealed in growth selected Macrobrachium rosenbergii. Aquac Int 27(2):497–508. https://doi.org/10.1007/s10499-018-0334-3
Hameed AS et al (2000) Tolerance of Macrobrachium rosenbergii to white spot syndrome virus. 183(3–4):207–213. https://doi.org/10.1016/S0044-8486(99)00305-1
Hu KJ, Leung PC (2004) Shrimp cathepsin L encoded by an intronless gene has predominant expression in hepatopancreas, and occurs in the nucleus of oocyte. Comp Biochem Physiol B Biochem Mol Biol 137(1):21–33. https://doi.org/10.1016/j.cbpc.2003.09.010
Hu KJ, Leung PC (2007) Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comp Biochem Physiol B-Biochem Mol Biol 146(1):69–80. https://doi.org/10.1016/j.cbpb.2006.09.010
Jung H et al (2013) Genes and growth performance in crustacean species: a review of relevant genomic studies in crustaceans and other taxa. Rev Aquac 5(2):77–110. https://doi.org/10.1111/raq.12005
Jung H et al (2014) A candidate gene association study for growth performance in an improved giant freshwater prawn (Macrobrachium rosenbergii) culture line. Mar Biotechnol 16(2):161–180. https://doi.org/10.1007/s10126-013-9555-7
Kawase T et al (2007) Alternative splicing due to an intronic SNP in HMSD generates a novel minor histocompatibility antigen. Blood 110(3):1055–1063. https://doi.org/10.1182/blood-2007-02-075911
Le Boulay C et al (1996) Cloning and expression of cathepsin L-like proteinases in the hepatopancreas of the shrimp Penaeus vannamei during the intermolt cycle. J Comp Physiol B 166(5):310–318
Li W et al (2010a) Molecular cloning, characterization, expression and activity analysis of cathepsin L in Chinese mitten crab, Eriocheir sinensis. Fish Shellfish Immunol 29(6):1010–1018. https://doi.org/10.1016/j.fsi.2010a.08.007
Li W et al (2010b) Molecular cloning, characterization and expression analysis of cathepsin C gene involved in the antibacterial response in Chinese mitten crab, Eriocheir sinensis. Dev Comp Immunol 34(11):1170–1174. https://doi.org/10.1016/j.dci.2010b.06.011
Liu J et al (2006) Cathepsin L function in insect moulting: molecular cloning and functional analysis in cotton bollworm, Helicoverpa armigera. Insect Mol Biol 15(6):823–834. https://doi.org/10.1111/j.1365-2583.2006.00686.x
Mercer TR et al (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3):155–159. https://doi.org/10.1038/nrg2521
Moyer RA et al (2011) Intronic polymorphisms affecting alternative splicing of human dopamine D2 receptor are associated with cocaine abuse. Neuropsychopharmacology 36(4):753–762. https://doi.org/10.1038/npp.2010.208
Nair CM, Salin KR (2012) Current status and prospects of farming the giant river prawn Macrobrachium rosenbergii (De Man) and the monsoon river prawn Macrobrachium malcolmsonii in India. Aquac Res 43(7):999–1014. https://doi.org/10.1111/j.1365-2109.2011.03074.x
Nguyen MT et al (2010) Single nucleotide polymorphisms in the actin and crustacean hyperglycemic hormone genes and their correlation with individual growth performance in giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 301(1–4):7–15. https://doi.org/10.1016/j.aquaculture.2010.02.001
Purcell S et al (2007) PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81(3):559–575. https://doi.org/10.1086/519795
Qian Z et al (2013) PCR-SSCP Polymorphism of CTSL gene and its correlation with growth traits of Litopenaeus vannamei and the different mRNA. expressions of CTSL. Acta Oceanol Sin 35(06):121–127. https://doi.org/10.3969/j.issn.0253-4193.2013.06.012
Ranjeet K, Kurup B (2002) Heterogeneous individual growth of Macrobrachium rosenbergii male morphotypes. Naga the ICLARM Q 25(2):13–18. https://doi.org/10.1111/are.12823
Tidwell JH (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii De Man 1879 in the United States. Aquac Res 43(7):1023–1028. https://doi.org/10.1111/j.1365-2109.2012.03130.x
Uszczynska-Ratajczak B et al (2018) Towards a complete map of the human long non-coding RNA transcriptome. Nat Rev Genet 19(9):535–548. https://doi.org/10.1038/s41576-018-0017-y
Wang Y et al (1998) "Experimental infection of white spot baculovirus in some cultured and wild decapods in Taiwan. Aquaculture 164(1–4):221–231. https://doi.org/10.1016/s0044-8486(98)00188-4
**ngjiang B et al (2008) Recombinant expression and tissue distribution of cathepsin L from Chinese shrimp Fenneropenaeus chinensis. J Fish Sci China 15(6):910–916
Yang G et al (2012) Current status of the giant freshwater prawn (Macrobrachium rosenbergii) industry in China, with special reference to live transportation. Aquac Res 43(7):1049–1055. https://doi.org/10.1111/j.1365-2109.2011.03009.x
Yang Z et al (2012) SNP identification and allelic-specific PCR markers development for TaGW2, a gene linked to wheat kernel weight. Theor Appl Genet 125(5):1057–1068. https://doi.org/10.1007/s00122-012-1895-6
Yoganandhan K, Hameed AS (2007) Tolerance to white spot syndrome virus (WSSV) in the freshwater prawn Macrobrachium rosenbergii is associated with low VP28 envelope protein expression. Dis Aquat Org 73(3):193–199. https://doi.org/10.3354/dao073193
Yuan R et al (2017) Phenomenon and research progress on prevention and control of ‘Iron Shell’ in giant freshwater prawn Macrobrachium rosenbergii. Fish Sci 36(03):383–390. https://doi.org/10.16378/j.cnki.1003-1111.2017.03.022
Zhong P et al (2019) Potential involvement of a DMRT family member (Mr-Dsx) in the regulation of sexual differentiation and moulting in the giant river prawn Macrobrachium rosenbergii Aquac Res 50(10):3037–3049. https://doi.org/10.1111/are.14262
Zhou J et al (2017) The preliminary analysis of the reasons for the poor growth of Macrobrachium rosenbergii in pond. J Shanghai Ocean Univ 26(6):853–861
Acknowledgements
We thank Qun Jiang and **aojian Gao for their help in sampling. This study was supported by the Major Fishery Science and Technology Projects in Jiangsu Province (D2017-3) and the National Natural Science Foundation of China (31702004).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Our study on Giant freshwater prawn, Macrobrachium rosenbergii, was approved by the Animal Care and Use Committee of the Yangzhou University (ethical protocol code: YZUDWSY 2016-05-06), and all efforts were made to minimize suffering. For instance, sufficient dissolved oxygen was provided during the transport, and all experimental prawns were first anesthetized with MS-222 (2 g/L, Sigma) before sacrificing and handling.
Conflict of interest
No conflict of interest exits in the submission of this manuscript, and the manuscript is approved by all authors for publication.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(JPG 19.6 KB)
Rights and permissions
About this article
Cite this article
Du, X., Yan, X., Zhang, W. et al. A SNP in Cathepsin L is associated with carapace length trait in giant freshwater prawn Macrobrachium rosenbergii. Biologia 76, 3587–3593 (2021). https://doi.org/10.1007/s11756-021-00860-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00860-4