Skip to main content
SpringerLink
Log in

Genome-wide identification of MAPK cascade genes reveals the GhMAP3K14–GhMKK11–GhMPK31 pathway is involved in the drought response in cotton

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The mitogen-activated protein kinase (MAPK) cascade pathway, which has three components, MAP3Ks, MKKs and MPKs, is involved in diverse biological processes in plants. In the current study, MAPK cascade genes were identified in three cotton species, based on gene homology with Arabidopsis. Selection pressure analysis of MAPK cascade genes revealed that purifying selection occurred among the cotton species. Expression pattern analysis showed that some MAPK cascade genes differentially expressed under abiotic stresses and phytohormones treatments, and especially under drought stress. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) experiments showed extensive interactions between different MAPK cascade proteins. Virus-induced gene silencing (VIGS) assays showed that some MAPK cascade modules play important roles in the drought stress response, and the GhMAP3K14–GhMKK11–GhMPK31 signal pathway was demonstrated to regulate drought stress tolerance in cotton. This study provides new information on the function of MAPK cascade genes in the drought response, and will help direct molecular breeding for improved drought stress tolerance in cotton.

Key message

Following a comprehensive analysis of MAPK cascade genes in cotton, we show that the GhMAP3K14–GhMKK11–GhMPK31 pathway is involved in the response to drought stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Batistič O, Sorek N, Schültke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362

    PubMed  PubMed Central  Google Scholar 

  • Benhamman R, Bai F, Drory SB, Loubert-Hudon A, Ellis B, Matton DP (2017) The Arabidopsis mitogen-activated protein kinase kinase kinase 20 (MKKK20) acts upstream of MKK3 and MPK18 in two separate signaling pathways involved in root microtubule functions. Front Plant Sci 8:1352

    PubMed  PubMed Central  Google Scholar 

  • Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106:8067–8072

    CAS  PubMed  Google Scholar 

  • Cai G, Wang G, Wang L, Liu Y, Pan J, Li D (2014) A maize mitogen-activated protein kinase kinase, ZmMKK1, positively regulated the salt and drought tolerance in transgenic Arabidopsis. J Plant Physiol 171:1003–1016

    CAS  PubMed  Google Scholar 

  • Chen L, Hu W, Tan S, Wang M, Ma Z, Zhou S, Deng X, Zhang Y, Huang C, Yang G, He G (2012) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS ONE 7:e46744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    CAS  PubMed  Google Scholar 

  • Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52

    CAS  PubMed  Google Scholar 

  • de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21:677–685

    PubMed  Google Scholar 

  • Fan K, Li F, Chen J, Li Z, Lin W, Cai S, Liu J, Lin W (2018) Asymmetric evolution and expansion of the NAC transcription factor in polyploidized cotton. Front Plant Sci 9:47

    PubMed  PubMed Central  Google Scholar 

  • Furuya T, Matsuoka D, Nanmori T (2014) Membrane rigidification functions upstream of the MEKK1-MKK2-MPK4 cascade during cold acclimation in Arabidopsis thaliana. FEBS Lett 588:2025–2030

    CAS  PubMed  Google Scholar 

  • Gao W, Long L, Zhu L, Xu L, Gao W, Sun L, Liu L, Zhang X (2013) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to verticillium dahliae. Mol Cell Proteomics 12:3690–3703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grefen C, Blatt MR (2012) A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). Biotechniques 53:311–314

    CAS  PubMed  Google Scholar 

  • Gu Z, Gu L, Eils R, Schlesner M, Brors B (2014) Circlize implements and enhances circular visualization in R. Bioinformatics 30:2811–2812

    CAS  PubMed  Google Scholar 

  • Han S, Fang L, Ren X, Wang W, Jiang J (2015) MPK6 controls H2O2-induced root elongation by mediating Ca2+ influx across the plasma membrane of root cells in Arabidopsis seedlings. New Phytol 205:695–706

    CAS  PubMed  Google Scholar 

  • Hettenhausen C, Schuman MC, Wu J (2015) MAPK signaling: a key element in plant defense response to insects. Insect Sci 22:157–164

    CAS  PubMed  Google Scholar 

  • Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741

    CAS  PubMed  Google Scholar 

  • Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A (2018) Mitogen-activated protein kinase cascades in plant hormone signaling. Front Plant Sci 9:1387

    PubMed  PubMed Central  Google Scholar 

  • Jia H, Hao L, Guo X, Liu S, Yan Y, Guo X (2016a) A Raf-like MAPKKK gene, GhRaf19, negatively regulates tolerance to drought and salt and positively regulates resistance to cold stress by modulating reactive oxygen species in cotton. Plant Sci 252:267–281

    CAS  PubMed  Google Scholar 

  • Jia W, Li B, Li S, Liang Y, Wu X, Ma M, Wang J, Gao J, Cai Y, Zhang Y, Wang Y, Li J, Wang Y (2016b) Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating pin1 in Arabidopsis. PLoS Biol 14(9):e1002550

    PubMed  PubMed Central  Google Scholar 

  • Kong Q, Qu N, Gao M, Zhang Z, Ding X, Yang F, Li Y, Dong O, Chen S, Li X, Zhang Y (2012) The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24:2225–2236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  • Li F, Li M, Wang P, Cox K, Duan L, Dever J, Shan L, Li Z, He P (2017a) Regulation of cotton (Gossypium hirsutum) drought responses by mitogen-activated protein (MAP) kinase cascade-mediated phosphorylation of GhWRKY59. New Phytol 215:1462–1475

    CAS  PubMed  Google Scholar 

  • Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017b) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642

    CAS  PubMed  Google Scholar 

  • Li K, Yang F, Zhang G, Song S, Li Y, Ren D, Miao Y, Song C (2017c) AIK1, A mitogen-activated protein kinase, modulates abscisic acid responses through the MKK5-MPK6 kinase cascade. Plant Physiol 173:1391–1408

    CAS  PubMed  Google Scholar 

  • Li Y, Cai H, Liu P, Wang C, Gao H, Wu C, Yan K, Zhang S, Huang J, Zheng C (2017d) Arabidopsis MAPKKK18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun 484:292–297

    CAS  PubMed  Google Scholar 

  • Lin F, Jiang Y, Li J, Yan T, Fan L, Liang J, Chen Z, Xu D, Deng X (2018) B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation. Plant Cell 30:2006–2019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Long L, Gao W, Xu L, Liu M, Luo X, He X, Yang X, Zhang X, Zhu L (2013) GbMPK3, a mitogen-activated protein kinase from cotton, enhances drought and oxidative stress tolerance in tobacco. Plant Cell Tissue Organ Cult 116:153–162

    Google Scholar 

  • Lv Y, Guo Z, Li X, Ye H, Li X, Xiong L (2016) New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell Environ 39:556–570

    CAS  PubMed  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–326

    CAS  PubMed  Google Scholar 

  • Ning J, Li X, Hicks LM, Xiong L (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pitzschke A (2015) Modes of MAPK substrate recognition and control. Trends Plant Sci 20:49–55

    CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    CAS  PubMed  Google Scholar 

  • Qiu J, Zhou L, Yun B, Nielsen H, Fiil B, Petersen K, Mackinlay J, Loake G, Mundy J, Morris P (2008) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK (2010) In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res 17:139–153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    CAS  PubMed  Google Scholar 

  • Su SH, Bush SM, Zaman N, Stecker K, Sussman MR, Krysan P (2013) Deletion of a tandem gene family in Arabidopsis: increased MEKK2 abundance triggers autoimmunity when the MEKK1-MKK1/2-MPK4 signaling cascade is disrupted. Plant Cell 25:1895–1910

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H, Chen L, Li J, Hu M, Ullah A, He X, Yang X, Zhang X (2017) The JASMONATE ZIM-domain gene family mediates JA signaling and stress response in cotton. Plant Cell Physiol 58:2139–2154

    CAS  PubMed  Google Scholar 

  • Sun H, Hu M, Li J, Chen L, Li M, Zhang S, Zhang X, Yang X (2018) Comprehensive analysis of NAC transcription factors uncovers their roles during fiber development and stress response in cotton. BMC Plant Biol 18:150

    PubMed  PubMed Central  Google Scholar 

  • Takagi M, Hamano K, Takagi H, Morimoto T, Akimitsu K, Terauchi R, Shirasu K, Ichimura K (2019) Disruption of the MAMP-induced MEKK1-MKK1/MKK2-MPK4 pathway activates the TNL immune receptor SMN1/RPS6. Plant Cell Physiol 60:778–787

    CAS  PubMed  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl J, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    CAS  PubMed  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15:271–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Zhao L, Lu R, Li Y, Li X (2015) Cotton mitogen-activated protein kinase4 (GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses. Plant Cell Tissue Organ Cult 123:619–632

    CAS  Google Scholar 

  • Wang C, Lu W, He X, Wang F, Zhou Y, Guo X, Guo X (2016a) The cotton mitogen-activated protein kinase kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant Cell Physiol 57:1629–1642

    CAS  PubMed  Google Scholar 

  • Wang M, Yue H, Feng K, Deng P, Song W, Nie X (2016b) Genome-wide identification, phylogeny and expressional profiles of mitogen activated protein kinase kinase kinase (MAPKKK) gene family in bread wheat (Triticum aestivum L.). BMC Genomics 17:668

    PubMed  PubMed Central  Google Scholar 

  • Wang L, Hu W, Tie W, Ding Z, Ding X, Liu Y, Yan Y, Wu C, Peng M, Xu B, Jin Z (2017) The MAPKKK and MAPKK gene families in banana: identification, phylogeny and expression during development, ripening and abiotic stress. Sci Rep 7:1159

    PubMed  PubMed Central  Google Scholar 

  • Wang H, Gong M, Guo J, Xin H, Gao Y, Liu C, Dai D, Tang L (2018) Genome-wide identification of Jatropha curcas MAPK, MAPKK, and MAPKKK gene families and their expression profile under cold stress. Sci Rep 8:16163

    PubMed  PubMed Central  Google Scholar 

  • Wu P, Wang W, Li Y, Hou X (2017) Divergent evolutionary patterns of the MAPK cascade genes in Brassica rapa and plant phylogenetics. Hortic Res 4:17079

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451

    CAS  PubMed  Google Scholar 

  • Xu J, Zhang S (2015) Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20:56–64

    CAS  PubMed  Google Scholar 

  • Xu R, Duan P, Yu H, Zhou Z, Zhang B, Wang R, Li J, Zhang G, Zhuang S, Lyu J, Li N, Chai T, Tian Z, Yao S, Li Y (2018) Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11:860–873

    CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    CAS  PubMed  Google Scholar 

  • Yang M, Li C, Cai Z, Hu Y, Nolan T, Yu F, Yin Y, Xie Q, Tang G, Wang X (2017) SINAT E3 ligases control the light-mediated stability of the brassinosteroid-activated transcription factor BES1 in Arabidopsis. Dev Cell 41(47–58):e44

    Google Scholar 

  • Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773

    CAS  PubMed  Google Scholar 

  • Zhan H, Yue H, Zhao X, Wang M, Song W, Nie X (2017) Genome-wide identification and analysis of MAPK and MAPKK gene families in bread wheat (Triticum aestivum L.). Genes 8(10):284

    PubMed Central  Google Scholar 

  • Zhang L, Xi D, Li S, Gao Z, Zhao S, Shi J, Wu C, Guo X (2011) A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco. Plant Mol Biol 77:17–31

    CAS  PubMed  Google Scholar 

  • Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (2012) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–263

    CAS  PubMed  Google Scholar 

  • Zhang X, Wang L, Xu X, Cai C, Guo W (2014) Genome-wide identification of mitogen-activated protein kinase gene family in Gossypium raimondii and the function of their corresponding orthologs in tetraploid cultivated cotton. BMC Plant Biol 14:345

    PubMed  PubMed Central  Google Scholar 

  • Zhang L, Zhao H, Dong Q, Zhang Y, Wang Y, Li H, Xing G, Li Q, Dong Y (2015a) 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

    PubMed  PubMed Central  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, et al (2015b) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    CAS  PubMed  Google Scholar 

  • Zhang X, Xu X, Yu Y, Chen C, Wang J, Cai C, Guo W (2016) Integration analysis of MKK and MAPK family members highlights potential MAPK signaling modules in cotton. Sci Rep 6:29781

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Mi X, Chen C, Wang H, Guo W (2018) Identification on mitogen-activated protein kinase signaling cascades by integrating protein interaction with transcriptional profiling analysis in cotton. Sci Rep 8:8178

    PubMed  PubMed Central  Google Scholar 

  • Zhao C, Nie H, Shen Q, Zhang S, Lukowitz W, Tang D, McDowell JM (2014) EDR1 physically interacts with MKK4/MKK5 and negatively regulates a MAP kinase cascade to modulate plant innate immunity. PLoS Genet 10:e1004389

    PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by funding from the National Key Project of Research and the Development Plan (2016YFD0101006)

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Lin Chen, Heng Sun, Fengjiao Wang, Dandan Yue, Xiankun Shen, Weinan Sun, Xianlong Zhang & Xiyan Yang

Authors
  1. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fengjiao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dandan Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiankun Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weinan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xianlong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XY and XZ designed the project. LC performed experiments and wrote the manuscript. XY and HS revised the manuscript. FW, DY, XS and WS help performed VIGS and BiFC experiments.

Corresponding author

Correspondence to Xiyan Yang.

Ethics declarations

Conflicts of interest

All authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, L., Sun, H., Wang, F. et al. Genome-wide identification of MAPK cascade genes reveals the GhMAP3K14–GhMKK11–GhMPK31 pathway is involved in the drought response in cotton. Plant Mol Biol 103, 211–223 (2020). https://doi.org/10.1007/s11103-020-00986-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-00986-0

Keywords

Search

Navigation