Abstract
In this study, we identified three neuroparsin (NP) genes in Macrobrachium nipponense: Mn-NP1, Mn-NP2, and Mn-NP3, encoding 99, 100, and 101 amino acid proteins, respectively. Multiple sequence alignments showed that these genes contained 12 cysteine residues, of which 11 were at conserved positions. The total sequence identity between the genes was 47.5%, and they showed a high degree of sequence identity (> 54% similarity) with other crustacean genes. Phylogenetic tree analysis showed that Mn-NPs were clustered at different branches, indicating that Mn-NPs may have different functions. Tissue distribution data revealed that the three genes were present in males and females during the breeding and nonbreeding season, but their expression patterns differed. Mn-NP1 was highly expressed in the breeding season, in the male testis, and highly expressed in the nonbreeding season, in the female ovary. Mn-NP3 exhibited biased female expression in the breeding and nonbreeding season, with dominant expression in the ovary. All Mn-NPs were detected during embryo development, but with different expression patterns. These data indicated that Mn-NP1 may function during embryonic development, and that Mn-NP2 may be expressed during early embryo cell division, and late larval development. Mn-NP3 expression patterns reflected maternal inheritance, and may be associated with ovarian maturation. These expression data suggested that Mn-NP1 and Mn-NP2 are negatively correlated with ovarian development, with inhibition roles during this development. Mn-NP3 may be involved in vitellogenesis.
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References
Badisco L, Claeys I, Van LT, Van HM, Franssens V, Simonet G, Broeck JV (2007) Neuroparsins, a family of conserved arthropod neuropeptides. Gen Comp Endocrinol 153(1–3):64–71
Badisco L, Marchal E, Van Wielendaele P, Verlinden H, Vleugels R, Broeck JV (2011) RNA interference of insulin-related peptide and neuroparsins affects vitellogenesis in the desert locust. Schistocerca gregaria 32(3):573–580
Bao C, Yang Y, Huang H, Ye H (2015) Neuropeptides in the cerebral ganglia of the mud crab, Scylla paramamosain: transcriptomic analysis and expression profiles during vitellogenesis. Scient Rep 5:17055
Brown MR, Graf R, Swiderek KM, Fendley D, Stracker TH, Champagne DE, Lea AO (1998) Identification of a steroidogenic neurohormone in female mosquitoes. J Biol Chem 273(7):3967–3971
Claeys I, Simonet G, Van LT, De LA, Vanden Broeck J (2003) cDNA cloning and transcript distribution of two novel members of the neuroparsin family in the desert locust, Schistocerca gregaria. Insect Mol Biol 12:473–481
Claeys I, Simonet G, Breugelmans B, Van SS, Franssens V, Sas F, Vanden BJ (2005) Quantitative real-time RT-PCR analysis in desert locusts reveals phase dependent differences in neuroparsin transcript levels. Insect Mol Biol 14(4):415–422
Claeys I, Breugelmans B, Simonet G, Van SS, Sas F, De LA, Broeck JV (2006) Neuroparsin transcripts as molecular markers in the process of desert locust (Schistocerca gregaria) phase transition. Biochem Biophys Res Commun 341(2):599–606
Fu H, Jiang S, Xiong Y (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii) and the oriental river prawn (Macrobrachium nipponense) in China. Aquac Res 43(7):993–998
Girardie J, Girardie A, Huet JC, Pernollet JC (1989) Amino acid sequence of locust neuroparsins. FEBS Lett 245(1–2):4–8
Hu Y, Fu H, Qiao H, Sun S, Zhang W, Jin S, Wu Y (2018) Validation and evaluation of reference genes for quantitative real-time PCR in Macrobrachium Nipponense. Int J Mol Sci 19(8):2258
Janssen T, Claeys I, Simonet G, De LA, Girardie J, Broeck JV (2001) cDNA cloning and transcript distribution of two different neuroparsin precursors in the desert locust Schistocerca gregaria. Insect Mole Biol 10(2):183–189
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Marco HG, Anders L, Gäde G (2014) cDNA cloning and transcript distribution of two novel members of the neuroparsin peptide family in a hemipteran insect (Nezara viridula) and a decapod crustacean (Jasus lalandii). Peptides 53:97–105
Nagaraju GPC (2011) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214(1):3–16
Qiao H, Xiong Y, Zhang W, Fu H, Jiang S, Sun S, Gong Y (2015) Characterization, expression, and function analysis of gonad-inhibiting hormone in Oriental River prawn, Macrobrachium nipponense and its induced expression by temperature. Comp Biochem Physiol A Mol Integr Physiol 185:1–8
Qiao H, Fu H, Xiong Y, Jiang S, Sun S, Jin S, Wu Y (2017) Molecular insights into reproduction regulation of female Oriental River prawns Macrobrachium nipponense through comparative transcriptomic analysis. Scient Rep 7(1):12161
Suwansaard S, Thongbuakaew T, Wang T, Zhao M, Elizur A, Hanna PJ, Sretarugsa P, Cummins SF, Sobhon P (2015) In silico neuropeptidome of female Macrobrachium rosenbergii based on transcriptome and peptide mining of eyestalk, central nervous system and ovary. PLoS ONE 10(5):e0123848
Veenstra JA (2010) what the loss of the hormone neuroparsin in the melanogaster subgroup of Drosophila can tell us about its function. Insect Biochem Mol Biol 40(4):354–361
Xu L, Yang M, Fu H, Sun S, Qiao H, Zhang W (2018) Molecular cloning and expression of MnGST-1 and MnGST-2 from Oriental River Prawn, Macrobrachium nipponense, in response to hypoxia and reoxygenation. Int J Mol Sci 19(10):3102
Zhang YP, Qiao H, Zhang WY, Sun SM, Jiang SF, Gong YS, Fu HT (2013) Molecular cloning and expression analysis of two sex-lethal homolog genes during development in the oriental river prawn Macrobrachium nipponense. Gene Mole Res 12(4):4698–4711
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This research was supported by Central Public interest Scientific Institution Basal Research Fund CAFS (2019JBFM04;2020TD36); Grants from the National Key R&D Progrom of China (2018YFD0901303); Jiangsu Agricultural Industry Technology System (JATS [2020] 461); The New cultivar breeding Major Project of Jiangsu province (PZCZ201745); the China Agriculture Research System-48 (CARS-48).
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Qiao, H., Xiong, Y., Jiang, S. et al. Three neuroparsin genes from oriental river prawn, Macrobrachium nipponense, involved in ovary maturation. 3 Biotech 10, 537 (2020). https://doi.org/10.1007/s13205-020-02531-8
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DOI: https://doi.org/10.1007/s13205-020-02531-8