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Heat-stress induced expression of stress-inducible nucleotide exchange factor Fes1 in seagrass Zostera japonica

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Abstract

Seagrass meadows are among the four most productive marine natural ecosystems in the world. Zostera japonica (Z. japonica) is the most widely distributed species of seagrass in China. Nucleotide exchange factors (NEFs) promote the release of ADP during heat stress, accelerating the rate-limiting step of Heat shock protein 70 (Hsp70). Although NEFs play an important role in abiotic stress tolerance of plants, NEFs in seagrass have not been studied. In this study, we cloned Fes1 from Z. japonica (ZjFes1) by rapid amplification of the cDNA ends using RACE, and full length ZjFes1 was 1171 bp. It contained an 81 bp 5′-terminal untranslated region (UTR), 109 bp 3′-UTR and 981 bp open reading frame (ORF). The ORF (ZjFes1) was predicted to encode a polypeptide of 326 amino acids with theoretical molecular weight (MW) of 36.10 kDa and pI of 5.22. ZjFes1 shared 89% amino acid identity with Fes1 from Zostera marina (Z. marina). The transcriptional levels of ZjFes1 increased significantly 1 h after heat treatment. ZjFes1 was localized to the cytoplasm. Taken together, we found that ZjFes1 was a stress-inducible gene that may be involved in heat stress response. This study lays the foundation for further studies on the role of ZjFes1 in heat resistance.

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Data availability

All data generated or analyzed during this study are included in this published article. The nucleotide and deduced amino acid sequence of ZjFes1 was registered in the GenBank (No. MK124711).

References

  • Adams MP, Collier CJ, Uthicke S, Ow YX, Langlois L, O’Brien KR (2017) Model fit versus biological relevance: evaluating photosynthesis-temperature models for three tropical seagrass species. Sci Rep 7:39930. https://doi.org/10.1038/srep39930

    Article  CAS  Google Scholar 

  • Alberti S, Böhse K, Arndt V, Schmitz A, Höhfeld J (2004) The cochaperone HspBP1 inhibits the CHIP ubiquitin ligase and stimulates the maturation of the cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 15:4003

    Article  CAS  Google Scholar 

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201. https://doi.org/10.1093/bioinformatics/bti770

    Article  CAS  Google Scholar 

  • Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Protein Pept Lett 125:443

    CAS  Google Scholar 

  • Collier CJ et al. (2018) Losing a winner: thermal stress and local pressures outweigh the positive effects of ocean acidification for tropical seagrasses. New Phytol 219:1005–1017. https://doi.org/10.1111/nph.15234

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783

    Article  Google Scholar 

  • Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603

    Article  CAS  Google Scholar 

  • Gassler CS, Wiederkehr T, Brehmer D, Bukau B, Mayer MP (2001) Bag-1M accelerates nucleotide release for human Hsc70 and Hsp70 and can act concentration-dependent as positive and negative cofactor. J Biol Chem 276:32538–32544

    Article  CAS  Google Scholar 

  • Gowda NK, Kaimal JM, Masser AE, Kang W, Friedländer MR, Andréasson C (2016) Cytosolic splice isoform of Hsp70 nucleotide exchange factor Fes1 is required for the degradation of misfolded proteins in yeast. Mol Biol Cell 27:1210–1219

    Article  CAS  Google Scholar 

  • Harrison CJ, Hayerhartl M, Di ML, Hartl F, Kuriyan J (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276:431–435

    Article  CAS  Google Scholar 

  • Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919

    Article  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  Google Scholar 

  • Kabani M, Beckerich JM, Brodsky JL (2002a) Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 22:4677–4689

    Article  CAS  Google Scholar 

  • Kabani M, Mclellan C, Raynes DA, Guerriero V, Brodsky JL (2002b) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett 531:339–342

    Article  CAS  Google Scholar 

  • Levitt M, Gerstein M, Huang E, Subbiah S, Tsai J (1997) Protein folding: the endgame. Annu Rev Biochem 66:549

    Article  CAS  Google Scholar 

  • Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88:2874–2878

  • Livak K, Schmittgen T(2000) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△Ct method Methods 25:402–8

    Article  Google Scholar 

  • NK G, G K, MS F, RJ D, C A (2013) Hsp70 nucleotide exchange factor Fes1 is essential for ubiquitin-dependent degradation of misfolded cytosolic proteins. PNAS 110:5975–5980

    Article  Google Scholar 

  • Pascal B, Marco B, Torsten S (2011) Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27:343–350

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406

    CAS  Google Scholar 

  • Shomura Y et al. (2005a) Regulation of Hsp70 function by HspBP1: structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol Cell 17:367–379

    CAS  Google Scholar 

  • Shomura Y et al. (2005b) Regulation of Hsp70 function by HspBP1: structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol Cell 17:367–379

    CAS  Google Scholar 

  • Sondermann H, Scheufler C, Schneider C, Hohfeld J, Hartl FU, Moarefi I (2001) Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291:1553–1557

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121

    Article  CAS  Google Scholar 

  • Zhang JX et al. (2010) The role of Arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance. Plant J 62:539–548. https://doi.org/10.1111/j.1365-313X.2010.04173.x

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the Guangxi Key Laboratory of Mangrove Conservation and Utilization funds (GKLMC-16A01), the Basic Scientific Foundation of Guangxi Institite of Public Welfare Scientific Research (2018GMRC02), the Natural Science Foundation of Guangxi Province (2018GXNSFBA281062), the Distinguished Employment Offered Unit of Guangxi for Conservation and Ecological Monitoring of Mangroves and Seagrasses, the National Science & Technology Basic Work Program (2015FY110600) and the National Key Research and Development Program of China (2017YFC0506100). These funding bodies had no role in experimental design, collection, analysis, and interpretation of data, or in writing the paper.

Author contributions

SC designed the study and performed the laboratory experiments. GQ designed the fieldwork. SC wrote most of the paper. All authors reviewed and edited the paper.

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  1. Guangxi Key Lab of Mangrove Conservation and Utilization, Guangxi Mangrove Research Center, Guangxi Academy of Sciences, Beihai, 536007, Guangxi, China

    Siting Chen & Guanglong Qiu

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  1. Siting Chen
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  2. Guanglong Qiu
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Correspondence to Siting Chen.

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Chen, S., Qiu, G. Heat-stress induced expression of stress-inducible nucleotide exchange factor Fes1 in seagrass Zostera japonica. Ecotoxicology 29, 932–940 (2020). https://doi.org/10.1007/s10646-020-02185-5

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