Skip to main content
SpringerLink
Log in

GhMAPKKK49, a novel cotton (Gossypium hirsutum L.) MAPKKK gene, is involved in diverse stress responses

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

MAPK (mitogen-activated protein kinase) family plays diverse roles in plant signal transduction and response to abiotic stress. In this study, we isolated a novel MAPKKK gene, GhMAPKKK49 from cotton (Gossypium hirsutum L.). The full-length cDNA of GhMAPKKK49 is 1,056 bp, encoding a protein of 351 amino acids. This protein contains a kinase catalytic domain, composed of an ATP binding site, a Ser/Thr kinase active site and a conserved Raf motif. The alignment analysis revealed a high sequence similarity of GhMAPKKK49 and other plant MAPKKK proteins. Our results indicated a constitutive expression of GhMAPKKK49 in roots, stems, and leaves. The expression of GhMAPKKK49 transcripts was found to be enhanced by abiotic salt, drought and wounding stresses but not the biotic stress of Ralstonia solanacearum or Rhizoctonia solani infection. Furthermore, real-time PCR showed that GhMAPKKK49 is upregulated in response to the application of various signaling molecules, including abscisic acid (ABA), hydrogen peroxide (H2O2), gibberellins (GAs), methyl jasmonate (MeJA), salicylic acid (SA), 6-benzylaminopurine (6-BA), a-naphthylacetic acid (NAA) and ethylene (ET). Furthermore, we demonstrate that GhMAPKKK49 interacts with GhMAPKK4 and GhMAPKK9. Give all that, GhMAPKKK49 may responds to various stresses and may involved in the ABA-, JA-, ET-, SA- and H2O2-mediated signaling pathways.

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
Fig. 6

Similar content being viewed by others

References

  • Alvarez ME (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol 44:429–442

    Article  CAS  PubMed  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    Article  CAS  PubMed  Google Scholar 

  • Galletti R, Ferrari S, De Lorenzo G (2011) Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide-or flagellin-induced resistance against Botrytis cinerea. Plant Physiol 157:804–814

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreisc M, Zhangd S, Hirte H, Wilsone C, Heberle-Borse E, Ellisf BE, Morrisg PC, Innesh RW, Eckeri JR, Scheelj D, Klessigk DF, Machidal Y, Mundym J, Ohashin Y, Walker JC (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  CAS  Google Scholar 

  • Jin H, Axtell MJ, Dahlbeck D, Ekwenna O, Zhang S, Staskawicz B, Baker B (2002) NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev Cell 3:291–297

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Ökrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424

    Article  CAS  PubMed  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441

    Article  CAS  PubMed  Google Scholar 

  • Kiegerl S, Cardinale F, Siligan C, Gross A, Baudouin E, Liwosz A, Eklof S, Till S, Bogre L, Hirt H et al (2000) SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stressinduced MAPK, SIMK. Plant Cell 12:2247–2258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim JA, Cho K, Singh R, Jung YH, Jeong SH, Kim SH, Lee JE, Cho YS, Agrawal GK, Rakwal R, Tamogami S, Kersten B, Jeon JS, An G, Jwa NS (2009) Rice OsACDR1 (Oryza sativa accelerated cell death, resistance 1) is a potential positive regulator of fungal disease resistance. Mol Cells 28:431–439

    Article  CAS  PubMed  Google Scholar 

  • Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, Yamane H, Miyao A, Takatsuji H, Takahashi A et al (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63:599–612

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leon J, Rojo E, Titarenko E, Sanchez-Serrano JJ (1998) Jasmonic acid-dependent and-independent wound signal transduction pathways are differentially regulated by Ca2+/calmodulin in Arabidopsis thaliana. Mol Gen Genet 258:412–419

    Article  CAS  PubMed  Google Scholar 

  • Li YZ, Zhang L, Wang X, Zhang W, Hao LL, Chu XQ, Guo XQ (2013) Cotton GhMPK6a negatively regulates osmotic tolerance and bacterial infection in transgenic Nicotiana benthamiana, and plays a pivotal role in development. FEBS J 280:5128–5144

    Article  CAS  PubMed  Google Scholar 

  • Li YZ, Zhang L, Lu WJ, Wang X, Wu CA, Guo XQ (2014) Overexpression of cotton GhMKK4 enhances disease susceptibility and affects abscisic acid, gibberellin and hydrogen peroxide signalling in transgenic Nicotiana benthamiana. Mol Plant Pathol 15:94–108

    Article  PubMed  Google Scholar 

  • Liu Y, Jin H, Yang KY, Kim CY, Baker B, Zhang S (2003) Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J 34:149–160

    Article  CAS  PubMed  Google Scholar 

  • Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler RON (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci 93:765–769

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959–26966

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346

    Article  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ning J, Zhang B, Wang N, Zhou Y, Xiong L (2011) Increased leaf angle1, a Raf-like MAPKKK that interacts with a nuclear protein family, regulates mechanical tissue formation in the lamina joint of rice. Plant Cell 23:4334–4347

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’donnell PJ, Calvert C, Atzorn R, Wasternack CHMO, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917

    Article  PubMed  Google Scholar 

  • Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  CAS  PubMed  Google Scholar 

  • Pedley KF, Martin GB (2004) Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem 279:49229–49235

    Article  CAS  PubMed  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    Article  CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JD (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    Article  CAS  PubMed  Google Scholar 

  • Shou H, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci 101:3298–3303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y (2003) NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 17:1055–1067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sunilkumar G, Campbell LM, Puckhaber L, Stipanovic RD, Rathore KS (2006) Engineering cotton seed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc Natl Acad Sci 103:18054–18059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tang D, Christiansen KM, Innes RW (2005) Regulation of plant disease resistance, stress responses, cell death, and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol 138:1018–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang XJ, Zhu SY, Lu YF, Zhao R, Xin Q, Wang XF, Zhang DP (2010) Two coupled components of the mitogen-activated protein kinase cascade MdMPK1 and MdMKK1 from apple function in ABA signal transduction. Plant Cell Physiol 51:754–766

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Xiao H, Chen G, Zhao X, Huang C, Chen C, Wang F (2011) Isolation of high-quality RNA from Reaumuria soongorica, a desert plant rich in secondary metabolites. Mol Biotechnol 48:165–172

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283:26996–27006

    Article  CAS  PubMed  Google Scholar 

  • Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci 98:741–746

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yin Z, Wang J, Wang D, Fan W, Wang S, Ye W (2013) The MAPKKK gene family in Gossypium raimondii: genome-wide identification, classification and expression analysis. Int J Mol Sci 14:18740–18757

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu F, Guo R, Wu C, Li H, Guo X (2012) Molecular cloning and expression characteristics of a novel MAPKKK gene, GhCTR1, from cotton (Gossypium hirsutum L.). S Afr J Bot 78:211–219

    Article  CAS  Google Scholar 

  • Zhang L, Li Y, Lu W, Meng F, Wu CA, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. J Exp Bot: ers086

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China [Grant Number 31171837; 31471424] and Tianjin Research Program of Application Foundation and Advanced Technology [11JCYBJC12400].

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, 271018, Shandong, People’s Republic of China

    Liu Dongdong, Zhu Ming, Hao Lili, Chen Xiaobo, Guo Xingqi & Li Han

  2. School of Medicine, Nankai University, 94 Weijin Road, Tianjin, 300071, People’s Republic of China

    Gao Yang

Authors
  1. Liu Dongdong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhu Ming
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hao Lili
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chen Xiaobo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gao Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guo Xingqi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Li Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li Han.

Additional information

Communicated by M. Stobiecki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dongdong, L., Ming, Z., Lili, H. et al. GhMAPKKK49, a novel cotton (Gossypium hirsutum L.) MAPKKK gene, is involved in diverse stress responses. Acta Physiol Plant 38, 13 (2016). https://doi.org/10.1007/s11738-015-2029-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-015-2029-y

Keywords

Search

Navigation