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Identification of an inositol-3-phosphate synthase 1-B gene (AccIPS1-B) from Apis cerana cerana and its role in abiotic stress

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Cell Stress and Chaperones Aims and scope

Abstract

Inositol phosphate synthase (IPS) is a rate-limiting enzyme in myo-inositol biosynthesis, which can regulate stress responses in plants and animals. However, there are few studies on the function of IPS in insects, especially in Apis cerana cerana. In this study, the inositol-3-phosphate synthase 1-B gene (AccIPS1-B) was isolated from Apis cerana cerana, and its connection to antioxidant defence was investigated. The open reading frame of AccIPS1-B was 1542 bp, encoding a 513 amino acid polypeptide. Quantitative real-time PCR analysis revealed that the expression level of AccIPS1-B was highest in pupae of Apis cerana cerana, and it was expressed at higher levels in the thorax than in other tissues tested. Moreover, the expression of AccIPS1-B was significantly upregulated by abiotic stresses. The recombinant AccIPS1-B also displayed significant tolerance to cumene hydroperoxide and HgCl2. In addition, knockdown of AccIPS1-B significantly suppressed the expression of most of the antioxidant genes and decreased the antioxidant enzymatic activities of SOD, POD, and GST. Taken together, these findings indicate that AccIPS1-B may be involved in the response to antioxidant defence and development in Apis cerana cerana.

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References

  • Butzin NC, Lapierre P, Green AG, Swithers KS, Gogarten JP, Noll KM (2013) Reconstructed ancestral myo-inositol-3-phosphate synthases indicate that ancestors of the thermococcales and thermotoga species were more thermophilic than their descendants. PLoS One 8:e84300

    Article  Google Scholar 

  • Cadet J, Sage E, Thierry D (2005) Ultraviolet radiation-mediated damage to cellular DNA. Mutat Res 571:3–17

    Article  CAS  Google Scholar 

  • Chen X, Yao P, Chu X, Hao L, Guo X, Xu B (2015) Isolation of arginine kinase from Apis cerana cerana and its possible involvement in response to adverse stress. Cell Stress Chaperones 20:169–183

    Article  CAS  Google Scholar 

  • Chen C, Chen K, Su T, Zhang B, Li G, Pan J, Si M (2018) Myo-inositol-1-phosphate synthase (Ino-1) functions as a protection mechanism in Corynebacterium glutamicum under oxidative stress. Microbiologyopen 1:e721

    Google Scholar 

  • Culbertson MR, Donahue TF, Henry SA (1976) Control of inositol biosynthesis in Saccharomyces cerevisiae: inositol-phosphate synthetase mutants. J Bacteriol 126(1):243–250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deranieh RM, He Q, Caruso JA, Greenberg ML (2013) Phosphorylation regulates myo-inositol-3-phosphate synthase: a novel regulatory mechanism of inositol biosynthesis. J Bio Chem 288:26822–26833

    Article  CAS  Google Scholar 

  • Donahue TF, Henry SA (1981) Inositol mutants of saccharomyces cerevisiae: mapping the ino1 locus and characterizing alleles of the ino1, ino2 and ino4 loci. Genetics 98(3):491–503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frej AD, Clark J, Le Roy CI, Lilla S, Thomason PA, Otto GP, ChurchillG IRH, Claus SP, Hawkins P, Stephens L, Williams RS (2016) The inositol-3-phosphate synthase biosynthetic enzyme has distinct catalytic and metabolic roles. Mol Cell Bio 36:1464–1479

    Article  CAS  Google Scholar 

  • Huang X, Hernick M (2015) Recombinant expression of a functional myo-inositol-1-phosphate synthase (MIPS) in Mycobacterium smegmatis. Protein J 34:380–390

    Article  CAS  Google Scholar 

  • Jia H, Sun R, Shi W, Yan Y, Li H, Guo X, Xu B (2014) Characterization of a mitochondrial manganese superoxide dismutase gene from Apis cerana cerana and its role in oxidative stress. J Insect Physio 60:68–79

    Article  CAS  Google Scholar 

  • Jia H, Ma M, Zhai N, Liu Z, Wang H, Guo X, Xu B (2017) Roles of a mitochondrial AccSCO2 gene from Apis cerana cerana in oxidative stress responses. J Inorg Biochem 175:9–15

    Article  CAS  Google Scholar 

  • Ju S, Shaltiel G, Shamir A, Agam G, Greenberg ML (2004) Human 1-D-myo-inositol-3-phosphate synthase is functional in yeast. J Bio Chem 279:21759–21765

    Article  CAS  Google Scholar 

  • Kaur H, Verma P, Petla BP, Rao V, Saxena SC, Majee M (2013) Ectopic expression of the ABA-inducible dehydration-responsive chickpeal-myo-inositol 1-phosphate synthase 2 (CaMIPS2) in Arabidopsis enhances tolerance to salinity and dehydration stress. Planta 237:321–335

    Article  CAS  Google Scholar 

  • Kottuparambil S, Shin W, Brown MT, Han T (2012) UV-B affects photosynthesis, ROS production and motility of the freshwater flagellate, Euglena agilis Carter. Aquat Toxicol 122-123:206–213

    Article  CAS  Google Scholar 

  • Kusuda H, Koga W, Kusano M, Oikawa A, Saito K, Hirai MY, Yoshida KT (2015) Ectopic expression of myo-inositol 3-phosphate synthase induces a wide range of metabolic changes and confers salt tolerance in rice. Plant Sci 232:49–56

    Article  CAS  Google Scholar 

  • Kuwano M, Mimura T, Takaiwa F, Yoshida KT (2010) Generation of stable ‘low phytic acid’ transgenic rice through antisense repression of the 1D-myo-inositol 3-phosphate synthase gene (RINO1) using the 18-kDa oleosin promoter. Plant Biotechnol J 7:96–105

    Article  Google Scholar 

  • Li T, Sun Y, Ruan Y, Xu L, Hu Y, Hao Z, Zhang X, Li H, Wang Y, Yang L, Chen B (2016) Potential role of D-myo-inositol-3-phosphate synthase and 14-3-3 genes in the crosstalk between Zea mays and Rhizophagus intraradices under drought stress. Mycorrhiza 26:879–893

    Article  CAS  Google Scholar 

  • Li M, Miao L, Chen Y, Hou H, Chen J (2018) Cloning of MIPS gene in large yellow croaker (Larimichthys crocea) and the expression analysis under cold treatments. J Agric Biotechnol 26:292–301

    Google Scholar 

  • Luo Y, Qin G, Zhang J, Liang Y, Song Y, Zhao M, Tsuge T, Aoyama T, Liu J, Gu H, Qu LJ (2011) D-myo-inositol-3-phosphate affects phosphatidylinositol mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 23:1352–1372

    Article  CAS  Google Scholar 

  • Lushchak VI (2010) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  Google Scholar 

  • Majumder AL, Chatterjee A, Ghosh DK, Majee M (2003) Diversification and evolution of L-myo-inositol 1-phosphate synthase. FEBS Lett 553(1):3–10

    Article  CAS  Google Scholar 

  • Meng F, Zhang Y, Liu F, Guo X, Xu B (2014) Characterization and mutational analysis of omega-class GST (GSTO1) from Apis cerana cerana, a gene involved in response to oxidative stress. PLoS One 9(3):e93100

    Article  Google Scholar 

  • Michelette ER, Soares AEE (1993) Characterization of preimaginal developmental stages in Africanized honey bee workers (Apis mellifera L). Apidologie 24:431–440

    Article  Google Scholar 

  • Parthasarathy RN, Lakshmanan J, Thangavel M, Seelan RS, Stagner JI, Janckila AJ, Vadna RE, Casanova MF, Parthasarathy LK (2013) Rat brain myo-inositol 3-phosphate synthase is a phosphoprotein. Mol Cell Biochem 378:83–89

    Article  CAS  Google Scholar 

  • Ravanat JL, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B Biol 63:88–102

    Article  CAS  Google Scholar 

  • Seelan RS, Pisano MM, Greene RM, Casanova MF, Parthasarathy RN (2011) Differential methylation of the gene encoding myo-inositol 3-phosphate synthase (Isyna1) in rat tissues. Epigenomics 3:111–124

    Article  CAS  Google Scholar 

  • Smith TK, Major LL (2011) Screening the maybridge rule of 3 fragment library for compounds that interact with the Trypanosoma brucei myo-inositol-3-phosphate synthase and/or show trypanocidal activity. Mol Bio Int 5:389–364

    Google Scholar 

  • Tan J, Wang C, Xiang B, Han R, Guo Z (2013) Hydrogen peroxide and nitric oxide mediated cold-induced and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ 36:288–299

    Article  CAS  Google Scholar 

  • Tang T, Huang D, Zhou C, Li X, Xie Q, Liu F (2012) Molecular cloning and expression patterns of copper/zinc superoxide dismutase and manganese superoxide dismutase in Musca domestica. Gene 505:211–220

    Article  CAS  Google Scholar 

  • Von KL, Crossgrove K, Von SD, Guild GM, Beckendorf SK (1994) The broad-complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J 13:3505–3516

    Article  Google Scholar 

  • Yan H, Jia H, Gao H, Guo X, Xu B (2013) Identification, genomic organization, and oxidative stress response of a sigma class glutathione S-transferase gene (AccGSTS1) in the honey bee, Apis cerana cerana. Cell Stress Chaperones 18:415–426

    Article  CAS  Google Scholar 

  • Yu F, Kang M, Meng F, Guo X, Xu B (2011) Molecular cloning and characterization of a thioredoxin peroxidase gene from Apis cerana cerana. Insect Mol Bio 20:367–378

    Article  Google Scholar 

  • Zhai H, Wang F, Si Z, Huo J, Xing L, An Y, He S, Liu Q (2016) A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnol J 14:592–602

    Article  CAS  Google Scholar 

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Funding

This work was financially supported by the Shandong Province Modern Agricultural Technology System Innovation Team Special Fund (SDAIT-24-04).

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Correspondence to Xingqi Guo or Qinghua Sun.

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Ni, Y., Li, G., Ji, X. et al. Identification of an inositol-3-phosphate synthase 1-B gene (AccIPS1-B) from Apis cerana cerana and its role in abiotic stress. Cell Stress and Chaperones 24, 1101–1113 (2019). https://doi.org/10.1007/s12192-019-01032-9

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  • DOI: https://doi.org/10.1007/s12192-019-01032-9

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