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DnaJs, the critical drivers of Hsp70s: genome-wide screening, characterization and expression of DnaJ family genes in Sorghum bicolor

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Abstract

The DnaJ/Hsp40s, are important components in the chaperone machine, and play pivotal roles in plant growth, development and stress tolerance. Sorghum, the semi-arid crop, is the drought resilient, model C4 crop. However, no reports of DnaJs have been available. Genome-wide analysis of Sorghum bicolor revealed 113 DnaJ/Hsp40 genes, classified into four groups; 8 genes in SbDnaJ-A class, 10 in SbDnaJ-B, 82 in SbDnaJ-C and 13 in SbDnaJ-D distributed unevenly on all the 10 chromosomes. Chromosomes 1 and 3 were found hot spots with 22 and 20 genes respectively. All genes displayed large number of introns, with an exception of 11 of the SbDnaJ-C which is devoid of introns. Out of 36 paralogous duplications, 7 tandem and 29 segmental duplications were noticed, indicating the major role of segmental duplications in the expansion. Analysis of digital data revealed tissue and stage-specific expressions. Transcriptional profiling of 12 selected genes representing all 4 classes revealed highly significant expression in leaf followed by root tissues. No expression was noticed in stems with an exception of SbDnaJ-C76. The SbDnaJ-A1, D1, and C subgroup genes displayed upregulation in roots, stems and leaves under cold, inferring the involvement of Hsp40s for cellular protection during cold stress. The results demonstrate that C76 and D1 are the candidate genes associated with multiple abiotic stresses. Present research furnishes valuable information about the role of sorghum DnaJs in abiotic stress response and establishes a foundation for understanding the molecular mechanisms associated with plant development and stress tolerance.

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Data availability

The datasets generated during and/or analyzed during the current study are available as the supplementary information.

References

  1. Qiu XB, Shao YM, Miao S, Wang L (2006) The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci 63:2560–2570. https://doi.org/10.1007/s00018-006-6192-6

    Article  CAS  PubMed  Google Scholar 

  2. Silver PA, Way JC (1993) Eukaryotic DnaJ homologs and the specificity of Hsp70 activity. Cell 74:5–6. https://doi.org/10.1016/0092-8674(93)90287-z

    Article  CAS  PubMed  Google Scholar 

  3. Fan F, Yang X, Cheng Y, Kang Y, Chai X (2017) The DnaJ gene family in pepper (Capsicum annuum L.): Comprehensive identification, characterization and expression profiles. Front Plant Sci 8:689. https://doi.org/10.3389/fpls.2017.00689

    Article  PubMed  PubMed Central  Google Scholar 

  4. Luo Y, Fang B, Wang W, Yang Y, Rao L, Zhang C (2019) Genome-wide analysis of the rice J-protein family: identification, genomic organization, and expression profiles under multiple stresses. 3 Biotech 9:358. https://doi.org/10.1007/s13205-019-1880-8

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kong F, Deng Y, Wang G, Wang J, Liang X, Meng Q (2014) LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J Integr Plant Biol 56:63–74. https://doi.org/10.1111/jipb.12119

    Article  CAS  PubMed  Google Scholar 

  6. Xia Z, Zhang X, Li J, Su X, Liu J (2014) Over expression of a tobacco J-domain protein enhances drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 83:100–106. https://doi.org/10.1016/j.plaphy.2014.07.023

    Article  CAS  PubMed  Google Scholar 

  7. Rajan VB, D’Silva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genomics 9:433–446. https://doi.org/10.1007/s10142-009-0132-0

    Article  CAS  PubMed  Google Scholar 

  8. Sarkar NK, Thapar U, Kundnani P, Panwar P, Grover A (2013) Functional relevance of J-protein family of rice (Oryza sativa). Cell Stress Chaperones 18:321–331. https://doi.org/10.1007/s12192-012-0384-9

    Article  CAS  PubMed  Google Scholar 

  9. Monaco MK, Stein J, Naithani S, Wei S, Dharmawardhana P, Kumari S, Amarsinghe V, Youens-Clark K, Thomason J, Preece J, Pasternak S, Olson A, Jiao Y, Lu Z, Bolser D, Kerhornou A, Staines D, WaltsB WuG, D’Eustachio P, Haw R, Croft D, Kersey PJ, Stein L, Jaiswal P, Ware D (2014) Gramene 2013: comparative plant genomics resources. Nucleic Acids Res 42(D1):D1193–D1199. https://doi.org/10.1093/nar/gkt1110

    Article  CAS  PubMed  Google Scholar 

  10. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32D:142–144. https://doi.org/10.1093/nar/gkh088

    Article  Google Scholar 

  11. Nagaraju M, Reddy PS, Anil Kumar S, Kumar A, Rajasheker G, Rao DM, Kavi Kishor PB (2020) Genome-wide identification and transcriptional profiling of small heat shock proten gene family under diverse abiotic stress conditions in Sorghum bicolor (L.). Int J Biol Macromol 142:822–834. https://doi.org/10.1016/j.ijbiomac.2019.10.023

    Article  CAS  PubMed  Google Scholar 

  12. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607

    Chapter  Google Scholar 

  13. Moller S, Croning MDR, Apweller R (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646–653. https://doi.org/10.1093/bioinformatics/17.7.646

    Article  CAS  PubMed  Google Scholar 

  14. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259

    Article  PubMed  PubMed Central  Google Scholar 

  15. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300. https://doi.org/10.1093/nar/27.1.297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Romauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612. https://doi.org/10.1093/nar/gkl315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta analysis of transcriptomes. Adv Bioinformatics. https://doi.org/10.1155/2008/420747

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf 13:134. https://doi.org/10.1186/1471-2105-13-134

    Article  CAS  Google Scholar 

  21. Reddy PS, Reddy DS, Sivasakthi K, Bhatnagar-Mathur P, Vadez V, Sharma KK (2016) Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Front Plant Sci 7:529. https://doi.org/10.3389/fpls.2016.00529

    Article  Google Scholar 

  22. Pfaffl WM, Horganl WG, Leo D (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 3:900. https://doi.org/10.1093/nar/30.9.e36

    Article  Google Scholar 

  23. Miernyk JA (2001) The J-domain proteins of Arabidopsis thaliana: an unexpectedly large and diverse family of chaperones. Cell Stress Chaperones 6:209–218. https://doi.org/10.1379/1466-1268(2001)006<0209:tjdpoa>2.0.co;2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Vembar SS, Jin Y, Brodsky JL, Hendershot LM (2009) The mammalian Hsp40 ERdj3 requires its Hsp70 interaction and substrate binding properties to complement various yeast Hsp40-dependent functions. J Biol Chem 284:32462–32471. https://doi.org/10.1074/jbc.M109.000729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Liu C, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M, Schroda M (2005) J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids. Mol Biol Cell 16:1165–1177. https://doi.org/10.1091/mbc.E04-08-0736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Angles F, Castanie-Cornet MP, Slama N, Dinclaux M, Cirinesi A, Portais J, Letisse F, Genevaux P (2017) Multilevel interaction of the DnaK/DnaJ (HSP70/HSP40) stress-responsive chaperone machine with the central metabolism. Sci. Rep 7:1–16. https://doi.org/10.1038/srep41341

    Article  CAS  Google Scholar 

  27. Hu L, Zhang Z, Xiang Z, Yang Z (2016) Exogenous application of citric acid ameliorates the adverse effect of heat stress in tall fescue (Lolium arundinaceum). Front Plant Sci 7:179. https://doi.org/10.3389/fpls.2016.00179

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wang G, Kong F, Zhang S, Meng X, Wang Y, Meng Q (2015) A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress. J Exp Bot 66:3027–3040. https://doi.org/10.1093/jxb/erv102

    Article  CAS  PubMed  Google Scholar 

  29. Valencia-Morales MD, Camas-Reyes JA, Cabrera-Ponce JL, Alvarez-Venegas R (2012) The Arabidopsis thaliana SET-domain containing protein ASHH1/SDG26 interacts with itself and with distinct histone lysine methyltransferases. J Plant Res 125:679–692. https://doi.org/10.1007/s10265-012-0485-7

    Article  CAS  Google Scholar 

  30. Feng K, Yu J, Cheng Y, Ruan M, Wang R, Ye Q, Zhou G, Li Z, Yao Z, Yang Y, Zheng Q, Wan H (2016) The SOD gene family in tomato: identification, phylogenetic relationships, and expression patterns. Front Plant Sci 7:1279. https://doi.org/10.3389/fpls.2016.01279

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

MN is thankful to the UGC, New Delhi, for providing fellowship. PBK is thankful to the Vignan’s Foundation for Science, Technology and Research, Guntur for providing Emeritus Fellowship.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Genetics, Osmania University, Hyderabad, 500 007, India

    M. Nagaraju, G. Rajasheker & D. Manohar Rao

  2. Advance Center for Computational & Applied Biotechnology, Uttarakhand Council for Biotechnology (UCB), Silk Park, Prem Nagar, Dehradun, 248 007, India

    Anuj Kumar

  3. Department of Biotechnology, Vignan’s Foundation for Science, Technology & Research, Vadlamudi, Guntur, Andhra Pradesh, 522 213, India

    P. B. Kavi Kishor

  4. Biochemistry Division, ICMR-National Institute of Nutrition, Hyderabad, 500 007, India

    M. Nagaraju

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Contributions

PBK, and DMR designed the experiments. MN implemented and collected the data. MN, AK, and RG performed experiments. MN, PBK, and DMR analyzed the results and prepared the manuscript. MN, AK, and PBK revised the manuscript. All authors have read and approved the manuscript.

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Correspondence to D. Manohar Rao or P. B. Kavi Kishor.

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Nagaraju, M., Kumar, A., Rajasheker, G. et al. DnaJs, the critical drivers of Hsp70s: genome-wide screening, characterization and expression of DnaJ family genes in Sorghum bicolor. Mol Biol Rep 47, 7379–7390 (2020). https://doi.org/10.1007/s11033-020-05793-w

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