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Genome-wide identification and expression analysis of the WNK kinase gene family in soybean

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Abstract

WNK kinases are a unique class of serine/threonine protein kinases that lack a conserved catalytic lysine residue in the kinase domain, hence the name WNK (with no K, i.e., lysine). WNK kinases are involved in various physiological processes in plants, such as circadian rhythm, flowering time, and stress responses. In this study, we identified 26 WNK genes in soybean and analyzed their phylogenetic relationships, gene structures, chromosomal distribution, cis-regulatory elements, expression patterns, and conserved protein motifs. The soybean WNK genes were unevenly distributed on 15 chromosomes and underwent 21 segmental duplication events during evolution. We detected 14 types of cis-regulatory elements in the promoters of the WNK genes, indicating their potential involvement in different signaling pathways. The transcriptome database revealed tissue-specific and salt stress-responsive expression of WNK genes in soybean, the second of which was confirmed by salt treatments and qRT-PCR analysis. We found that most WNK genes were significantly up-regulated by salt stress within 3 h in both roots and leaves, except for WNK5, which showed a distinct expression pattern. Our findings provide valuable insights into the molecular characteristics and evolutionary history of the soybean WNK gene family and lay a foundation for further analysis of WNK gene functions in soybean.

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References

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Feng R, Ren M, Lu L, Peng M, Guan X, Zhou D, Zhang M, Qi D, Li K, Tang W, Yun T, Chen Y, Wang F, Zhang D, Shen Q, Liang P, Zhang Y, Xie J (2019) Involvement of abscisic acid-responsive element-binding factors in cassava (Manihot esculenta) dehydration stress response. Sci Rep 9:12661

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Gill N, Findley S, Walling JG, Hans C, Ma J, Doyle J, Stacey G, Jackson SA (2009) Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol 151:1167–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Porras JL, Riaño-Pachón DM, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genom 8:260

    Article  Google Scholar 

  • Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. Faseb j 9:576–596

    Article  CAS  PubMed  Google Scholar 

  • Hong-Hermesdorf A, Brüx A, Grüber A, Grüber G, Schumacher K (2006) A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett 580:932–939

    Article  CAS  PubMed  Google Scholar 

  • Huang CL, Cha SK, Wang HR, Xie J, Cobb MH (2007) WNKs: protein kinases with a unique kinase domain. Exp Mol Med 39:565–573

    Article  CAS  PubMed  Google Scholar 

  • Kahle KT, Rinehart J, Ring A, Gimenez I, Gamba G, Hebert SC, Lifton RP (2006) WNK protein kinases modulate cellular Cl- flux by altering the phosphorylation state of the Na-K-Cl and K-Cl cotransporters. Physiology (bethesda) 21:326–335

    CAS  PubMed  Google Scholar 

  • Kumar K, Kumar M, Kim SR, Ryu H, Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar K, Raina SK, Sultan SM (2020) Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. J Plant Biochem BioT 29:700–714

    Article  CAS  Google Scholar 

  • Lallemand T, Leduc M, Landès C, Rizzon C, Lerat E (2020) An overview of duplicated gene detection methods: why the duplication mechanism has to be accounted for in their choice. Genes (basel) 11:1046

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Liu X, Zhao Y, Nie J, Yao X, Lv L, Yang J, Ma N, Guo Y, Li Y, Yang X, Lin T, Sui X (2022a) Alkaline α-galactosidase 2 (CsAGA2) plays a pivotal role in mediating source-sink communication in cucumber. Plant Physiol 189:1501–1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R, Vasupalli N, Hou D, Stalin A, Wei H, Zhang H, Lin X (2022b) Genome-wide identification and evolution of WNK kinases in Bambusoideae and transcriptional profiling during abiotic stress in Phyllostachys edulis. PeerJ 10:e12718

    Article  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma TL, Wu WH, Wang Y (2012) Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biol 12:161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manuka R, Saddhe AA, Kumar K (2015) Genome-wide identification and expression analysis of WNK kinase gene family in rice. Comput Biol Chem 59:56–66 (Pt A)

    Article  CAS  PubMed  Google Scholar 

  • Manuka R, Saddhe AA, Kumar K (2018) Expression of OsWNK9 in Arabidopsis conferred tolerance to salt and drought stress. Plant Sci 270:58–71

    Article  CAS  PubMed  Google Scholar 

  • Manuka R, Karle SB, Kumar K (2019) OsWNK9 mitigates salt and drought stress effects through induced antioxidant systems in Arabidopsis. Plant Physiol 24:168–181

    Article  CAS  Google Scholar 

  • McCormick JA, Ellison DH (2011) The WNKs: atypical protein kinases with pleiotropic actions. Physiol Rev 91:177–219

    Article  CAS  PubMed  Google Scholar 

  • Murakami-Kojima M, Nakamichi N, Yamashino T, Mizuno T (2002) The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana. Plant Cell Physiol 43:675–683

    Article  CAS  PubMed  Google Scholar 

  • Nakamichi N, Murakami-Kojima M, Sato E, Kishi Y, Yamashino T, Mizuno T (2002) Compilation and characterization of a novel WNK family of protein kinases in Arabidopsis thaliana with reference to circadian rhythms. Biosci Biotechnol Biochem 66:2429–2436

    Article  CAS  PubMed  Google Scholar 

  • Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, Yates JR, Schroeder JI (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299

    Article  CAS  PubMed  Google Scholar 

  • Papiernik SK, Grieve CM, Lesch SM, Yates SR (2005) Effects of salinity, imazethapyr, and chlorimuron application on soybean growth and yield. Commun Soil Sci Plan 36:951–967

    Article  CAS  Google Scholar 

  • Pei X, Wang X, Fu G, Chen B, Nazir MF, Pan Z, He S, Du X (2021) Identification and functional analysis of 9-cis-epoxy carotenoid dioxygenase (NCED) homologs in G. hirsutum. Int J Biol Macromol 182:298–310

    Article  CAS  PubMed  Google Scholar 

  • Richardson C, Alessi DR (2008) The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci 121:3293–3304

    Article  CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  ADS  CAS  PubMed  Google Scholar 

  • Sun Z, Feng Z, Ding Y, Qi Y, Jiang S, Li Z, Wang Y, Qi J, Song C, Yang S, Gong Z (2022) RAF22, ABI1 and OST1 form a dynamic interactive network that optimizes plant growth and responses to drought stress in Arabidopsis. Mol Plant 15:1192–1210

    Article  CAS  PubMed  Google Scholar 

  • Tang BL (2016) (WNK)ing at death: with-no-lysine (Wnk) kinases in neuropathies and neuronal survival. Brain Res Bull 125:92–98

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchiya T, Eulgem T (2010) The Arabidopsis defense component EDM2 affects the floral transition in an FLC-dependent manner. Plant J 62:518–528

    Article  CAS  PubMed  Google Scholar 

  • Uchida S, Sohara E, Rai T, Sasaki S (2014) Regulation of with-no-lysine kinase signaling by Kelch-like proteins. Biol Cell 106:45–56

    Article  CAS  PubMed  Google Scholar 

  • Urano D, Czarnecki O, Wang X, Jones AM, Chen JG (2015) Arabidopsis receptor of activated C kinase1 phosphorylation by with no lysine8 kinase. Plant Physiol 167:507–516

    Article  CAS  PubMed  Google Scholar 

  • Veríssimo F, Jordan P (2001) WNK kinases, a novel protein kinase subfamily in multi-cellular organisms. Oncogene 20:5562–5569

    Article  PubMed  Google Scholar 

  • Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:1–10

    Article  Google Scholar 

  • Villa F, Goebel J, Rafiqi FH, Deak M, Thastrup J, Alessi DR, van Aalten DM (2007) Structural insights into the recognition of substrates and activators by the OSR1 kinase. EMBO Rep 8:839–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Liu K, Liao H, Zhuang C, Ma H, Yan X (2008) The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol (stuttg) 10:548–562

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Suo H, Zheng Y, Liu K, Zhuang C, Kahle KT, Ma H, Yan X (2010) The soybean root-specific protein kinase GmWNK1 regulates stress-responsive ABA signaling on the root system architecture. Plant J 64:230–242

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Song L, Gong X, Xu J, Li M (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci 21:1446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Sun Z, Liu H, Yue L, Wang F, Liu S, Su B, Liu B, Kong F, Fang C (2023) Genome-wide identification and characterization of the soybean Snf2 gene family and expression response to rhizobia. Int J Mol Sci 24:7250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson FH, Disse-Nicodème S, Choate KA, Ishikawa K, Nelson-Williams C, Desitter I, Gunel M, Milford DV, Lipkin GW, Achard JM, Feely MP, Dussol B, Berland Y, Unwin RJ, Mayan H, Simon DB, Farfel Z, Jeunemaitre X, Lifton RP (2001) Human hypertension caused by mutations in WNK kinases. Science 293:1107–1112

    Article  CAS  PubMed  Google Scholar 

  • Xie M, Wu D, Duan G, Wang L, He R, Li X, Tang D, Zhao X, Liu X (2014) AtWNK9 is regulated by ABA and dehydration and is involved in drought tolerance in Arabidopsis. Plant Physiol Biochem 77:73–83

    Article  CAS  PubMed  Google Scholar 

  • Xu B, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, Cobb MH (2000) WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. J Biol Chem 275:16795–16801

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Liu K, Zheng Y, Wang Y, Wang J, Liao H (2013) Disruption of AtWNK8 enhances tolerance of Arabidopsis to salt and osmotic stresses via modulating proline content and activities of catalase and peroxidase. Int J Mol Sci 14:7032–7047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 32301822), the China Postdoctoral Science Foundation (Grant No. 2022M720882), the Innovation Research Project of Coarse Cereals Specialty in Guizhou Province [2019[4012]], and the Regional First-class Discipline of Ecology in Guizhou Province (XKTJ[2020]22).

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  1. Bohong Su and Tianli Ge contributed equally to this work.

Authors and Affiliations

  1. Guangzhou Key Laboratory of Crop Gene Editing, Guangdong Key Laboratory of Plant Adaptation and Molecular Design, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou, 510006, China

    Bohong Su, Tianli Ge, Yuhang Zhang, Jianhao Wang, Fan Wang, Baohui Liu, Fanjiang Kong & Zhihui Sun

  2. School of Ecological Engineering, Guizhou University of Engineering Science, Bijie, 551700, People’s Republic of China

    Tu Feng

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  1. Bohong Su
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Contributions

BS and ZS conceived and designed the research. BS and ZS performed the experiments and collected the data. JW and YZ supervised the experiments. BS wrote the manuscript. FK and BL modified manuscript. TG polished the manuscript. FW and TF polished the images. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Zhihui Sun.

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Su, B., Ge, T., Zhang, Y. et al. Genome-wide identification and expression analysis of the WNK kinase gene family in soybean. Mol Breeding 44, 16 (2024). https://doi.org/10.1007/s11032-024-01440-5

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