Genome-wide analysis of the HSP90 gene family and their roles in soybean growth and development

Document Type : Original research paper

Authors
Genetics and Agricultural Biotechnology Institute of Tabarestan (GABIT), Sari Agricultural Sciences and Natural Resources University (SANRU)
Abstract
Heat shock protein of 90 kDa or HSP90 plays an important dynamic role in regulating biotic and abiotic stresses through multiple functional mechanisms. The present study aimed to perform a comprehensive analysis of the HSP90 gene family in soybean. In total, 20 HSP90 genes from soybean were identified and showed unequal distribution on the 13 chromosomes. The evolutionary tree divided these genes into three main groups based on their subcellular localization. In Group I, nearly all of the HSP90 genes are distributed in the nucleus or cytoplasm. In Group II, the HSP90s were mostly classified in the endoplasmic reticulum. HSP90 genes were exclusively found in the mitochondria or chloroplast in Group III. Phylogenetic relationships have shown that genes in similar subgroups have the same exon-intron structure and number of introns. Glyma14g219700, Glyma17g258700, and Glyma07G207600 were identified as hub proteins based on their high degrees of interaction. In addition, Glyma02g302500, Glyma08g332900, Glyma14g219700, Glyma17g258700, and Glyma18g074100 genes displayed high expression levels in all of the tissues at different developmental stages. These findings provide a complete overview of the GmHSP90 gene family classification and evolution, which can help to identify the functional properties of the HSP90 genes in soybean growth and development.
Keywords

Appiah, C., Yang, Z.-F., He, J., Wang, Y., Zhou, J., Xu, W.-Z., Nie, G., and Zhu, Y.-Q. (2021). Genome-Wide identification of Hsp90 gene family in Perennial Ryegrass and expression analysis under various abiotic stresses. Plants 10(11): 2509.
Bai, J., Pennill, L.A., Ning, J., Lee, S.W., Ramalingam, J., Webb, C.A., Zhao, B., Sun, Q., Nelson, J.C., and Leach, J.E. (2002). Diversity in nucleotide binding site–leucine-rich repeat genes in cereals. Genome Res 12(12): 1871-1884.
Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., and Noble, W.S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: 202-208.
Bettaieb, I., Hamdi, J., and Bouktila, D. (2020). Genome-wide analysis of HSP90 gene family in the Mediterranean olive (Olea europaea subsp. europaea) provides insight into structural patterns, evolution and functional diversity. Physiol Mol Biol Plants 26(11): 2301-2318.
Brown, A.V., Conners, S.I., Huang, W., Wilkey, A.P., Grant, D., Weeks, N.T., Cannon, S.B., Graham, M.A., and Nelson, R.T. (2021). A new decade and new data at SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 49(D1): D1496-D1501.
Chaudhary, R., Baranwal, V.K., Kumar, R., Sircar, D., and Chauhan, H. (2019). Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development. Funct Integr Genomics 19(6): 1007-1022.
Chen, J., Gao, T., Wan, S., Zhang, Y., Yang, J., Yu, Y., and Wang, W. (2018). Genome-wide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis). Int J Mol Sci 19(9): 2633.
di Donato, M., and Geisler, M. (2019). HSP 90 and co‐chaperones: a multitaskers’ view on plant hormone biology. FEBS letters 593(13): 1415-1430.
Finn, R.D., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Mistry, J., Mitchell, A.L., Potter, S.C., Punta, M., Qureshi, M., and Sangrador-Vegas, A. (2015). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44: 279-285.
Gasteiger, E., Hoogland, C., Gattiker, A., Wilkins, M.R., Appel, R.D., and Bairoch, A. (2005). "Protein identification and analysis tools on the ExPASy server," in The proteomics protocols handbook, ed. J.M. Walker.  (New York City, New York, United States: Humana Press), 571-607.
Hashemipetroudi, S.H., Mohammadi, S., and Kuhlmann, M. (2019). Analysis of expression pattern of genome and analysis of HSP90 gene family in Aeluropus littoralis under salinity stress. Crop Breed J 11(31): 134-143.
Haxim, Y., Si, Y., Liu, X., Wen, X., Kahar, G., Ding, Y., Li, X., and Zhang, D. (2021). Genome-wide characterization of HSP90 gene family in Malus sieversii and their potential roles in response to Valsa mali infection. Forests 12(9): 1232.
Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C., and Nakai, K. (2007). WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: 585-587.
Hoter, A., El-Sabban, M.E., and Naim, H.Y. (2018). The HSP90 family: structure, regulation, function, and implications in health and disease. Int J Mol Sci 19(9): 2560.
Hu, B., Jin, J., Guo, A.-Y., Zhang, H., Luo, J., and Gao, G. (2014). GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8): 1296-1297.
Hu, W., Hu, G., and Han, B. (2009). Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176(4): 583-590.
Jing, W., Fangjun, T., Chengliang, L., Xilu, Z., Lijun, O., Juntawong, N., Fei, W., Chunhai, J., Xuexiao, Z., and Wenchao, C. (2020). Genome-wide identification and analysis of HSP90 gene family in pepper. Acta Horticulturae Sinica 47(4): 665.
Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., and Nuka, G. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9): 1236-1240.
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7): 1870-1874.
Letunic, I., Doerks, T., and Bork, P. (2014). SMART: recent updates, new developments and status in 2015. Nucleic acids res 43(D1): D257-D260.
Li, W., Chen, Y., Ye, M., Wang, D., and Chen, Q. (2020). Evolutionary history of the heat shock protein 90 (Hsp90) family of 43 plants and characterization of Hsp90s in Solanum tuberosum. Mol Biol Rep 47(9): 6679-6691.
Mishra, R.C., and Grover, A. (2016). Constitutive over-expression of rice ClpD1 protein enhances tolerance to salt and desiccation stresses in transgenic Arabidopsis plants. Plant Sci 250: 69-78.
Mishra, S., Chaudhary, R., Pandey, B., Singh, G., and Sharma, P. (2023). Genome-wide identification and expression analysis of the GRAS gene family under abiotic stresses in wheat (Triticum aestivum L.). Sci Rep 13(1): 18705.
Pearl, L.H., and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75(1): 271-294.
Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life 59(10): 1640-1648.
Prasad, B.D., Goel, S., and Krishna, P. (2010). In silico identification of carboxylate clamp type tetratricopeptide repeat proteins in Arabidopsis and rice as putative co-chaperones of Hsp90/Hsp70. Plos One 5(9): e12761.
Reddy, R.K., Chaudhary, S., Patil, P., and Krishna, P. (1998). The 90 kDa heat shock protein (hsp90) is expressed throughout Brassica napus seed development and germination. Plant Sci 131(2): 131-137.
Sable, A., Rai, K.M., Choudhary, A., Yadav, V.K., Agarwal, S.K., and Sawant, S.V. (2018). Inhibition of heat shock proteins HSP90 and HSP70 induce oxidative stress, suppressing cotton fiber development. Sci Rep 8(1): 1-17.
Sangster, T.A., and Queitsch, C. (2005). The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr Opin Plant Biol 8(1): 86-92.
Sarkar, N.K., Kim, Y.-K., and Grover, A. (2009). Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genom 10(1): 1-18.
Scherf, U., Ross, D.T., Waltham, M., Smith, L.H., Lee, J.K., Tanabe, L., Kohn, K.W., Reinhold, W.C., Myers, T.G., and Andrews, D.T. (2000). A gene expression database for the molecular pharmacology of cancer. Nat Genet 24(3): 236-244.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11): 2498-2504.
Shelke, D.B., Chambhare, M.R., Nikalje, G.C., and Nikam, T. (2023). Improvement of soybean crop for yield, stress tolerance, and value-added products using a transgenic approach. Adv Agric 2023. doi: 10.1155/2023/8166928.
Song, Z., Pan, F., Yang, C., Jia, H., Jiang, H., He, F., Li, N., Lu, X., and Zhang, H. (2019). Genome-wide identification and expression analysis of HSP90 gene family in Nicotiana tabacum. BMC Genet 20(1): 1-12.
Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N.T., Morris, J.H., and Bork, P. (2019). STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1): D607-D613.
Vabulas, R.M., Raychaudhuri, S., Hayer-Hartl, M., and Hartl, F.U. (2010). Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb Perspect Biol 2(12): a004390.
Vaughan, M.M., Block, A., Christensen, S.A., Allen, L.H., and Schmelz, E.A. (2018). The effects of climate change associated abiotic stresses on maize phytochemical defenses. Phytochem Rev 17: 37-49.
Voorrips, R. (2002). MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1): 77-78.
Wang, W., Vinocur, B., Shoseyov, O., and Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9(5): 244-252.
Zhang, J., Li, J., Liu, B., Zhang, L., Chen, J., and Lu, M. (2013). Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genom 14(1): 532.
Zhang, K., He, S., Sui, Y., Gao, Q., Jia, S., Lu, X., and Jia, L. (2021). Genome-wide characterization of HSP90 gene family in cucumber and their potential roles in response to abiotic and biotic stresses. Front Genet 12: 584886.
Zhang, L., Zhao, H.-K., Dong, Q.-l., Zhang, Y.-Y., Wang, Y.-M., Li, H.-Y., Xing, G.-J., Li, Q.-Y., and Dong, Y.-S. (2015). Genome-wide analysis and expression profiling under heat and drought treatments of HSP70 gene family in soybean (Glycine max L.). Front Plant Sci 6: 773.
Zhang, M., Shen, Z., Meng, G., Lu, Y., and Wang, Y. (2017). Genome-wide analysis of the Brachypodium distachyon (L.) P. Beauv. Hsp90 gene family reveals molecular evolution and expression profiling under drought and salt stresses. PloS One 12(12): e0189187.
Volume 11, Issue 2
December 2023
Pages 119-132

  • Receive Date 06 June 2022
  • Revise Date 08 May 2024
  • Accept Date 16 May 2024
  • First Publish Date 16 May 2024