Skip to main content
Log in

Genome-wide identification of the mitogen-activated protein kinase (MAPK) family in cotton (Gossypium hirsutum) reveals GhMPK6 involved in fiber elongation

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinases (MAPKs) are important in regulating plant development as well as stress response. In this study, we genome-widely identified 56 MAPK genes in upland cotton. These MAPK genes unequally distribute on 22 chromosomes of cotton genome, but no MAPK gene is located on At_Chr6, Dt_Chr6, At_Chr13 and Dt_Chr13. The exons and introns in GhMAPK gene family vary widely at the position, number and length. Furthermore, GhMAPK family can be divided into 4 groups (A, B, C and D), and the TEY type of T-loop exists in three groups (A, B and C), but the TDY type of T-loop is only in group D. Further study revealed that some GhMAPK genes (including GhMPK6) are preferentially expressed in elongating fibers. GhMPK6 maintains a high phosphorylation level in elongating fibers, and its phosphorylation was enhanced in fibers by phytohormones brassinosteroid (BR), ethylene and indole-3-acetic acid (IAA). Additionally, GhMPK6 could interact with GhMKK2-2 and GhMKK4, suggesting that GhMKK2-2/4-GhMPK6 module may be involved in phosphorylation of its downstream proteins for regulating fiber elongation of cotton.

Key message

56 MAPK genes were identified in upland cotton genome, and unequally distribute on 22 chromosomes of cotton genome. They can be divided into 4 groups, and the TEY type of T-loop exists in A, B and C groups, but the TDY type of T-loop is only in group D. Furthermore, GhMPK6 may be involved in phosphorylation of its downstream proteins for regulating fiber elongation of cotton.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Asif MH, Lakhwani D, Pathak S, Bhambhani S, Bag SK, Trivedi PK (2014) Genome-wide identification and expression analysis of the mitogen-activated protein kinase gene family from banana suggest involvement of specific members in different stages of fruit ripening. Funct Integr Genomics 14:161–175

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36

    CAS  PubMed  Google Scholar 

  • Beasley CA, Ting IP (1974) Effects of plant growth substances on in vitro fiber development from unfertilized cotton ovules. Am J Bot 61:188–194

    Article  CAS  Google Scholar 

  • Casar B, Pinto A, Crespo P (2009) ERK dimers and scaffold proteins: unexpected partners for a forgotten (cytoplasmic) task. Cell Cycle 8:1007–1013

    Article  CAS  PubMed  Google Scholar 

  • Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding H, He J, Wu Y, Wu X, Ge C, Wang Y, Zhong S, Peiter E, Liang J, Xu W (2018) The Tomato Mitogen-Activated Protein Kinase SlMPK1 Is as a Negative Regulator of the High-Temperature Stress Response. Plant Physiol 177:633–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djonović S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact 19:838–853

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR (2015) HMMER web server: 2015 update. Nucleic Acids Res 43(W1):W30–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Formstecher E, Ramos JW, Fauquet M, Calderwood DA, Hsieh JC, Canton B, Nguyen XT, Barnier JV, Camonis J, Ginsberg MH, Chneiweiss H (2001) PEA-15 mediates cytoplasmic sequestration of ERK MAP kinase. Dev Cell 1:239–250

    Article  CAS  PubMed  Google Scholar 

  • Fukuda M, Gotoh I, Gotoh Y, Nishida E (1996) Cytoplasmic localization of mitogen-activated protein kinase kinase directed by its NH2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J Biol Chem 271:20024–20028

    Article  CAS  PubMed  Google Scholar 

  • Gawroński P, Witoń D, Vashutina K, Bederska M, Betliński B, Rusaczonek A, Karpiński S (2014) Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol Plant 7:1151–1166

    Article  PubMed  CAS  Google Scholar 

  • Gong SY, Huang GQ, Sun X, Qin LX, Li Y, Zhou L, Li XB (2014) Cotton KNL1, encoding a class II KNOX transcription factor, is involved in regulation of fibre development. J Exp Bot 65:4133–4147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262

    Article  CAS  PubMed  Google Scholar 

  • Haigler CH, Betancur L, Stiff MR, Tuttle JR (2012) Cotton fiber: a powerful single-cell model for cell wall and cellulose research. Front Plant Sci 3:104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Li H, Hutchison CE, Laskey J, Kieber JJ (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J 33:221–233

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Triplett BA (2001) Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol 127:1361–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim JY, Chung WS (2017) Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res 45:6613–6627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JS, Wang S, Sritubtim S, Chen JG, Ellis BE (2009) Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J 57:975–985

    Article  CAS  PubMed  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20:116–122

    Article  CAS  PubMed  Google Scholar 

  • Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49–139

    Article  CAS  PubMed  Google Scholar 

  • Li XB, Fan XP, Wang XL, Cai L, Yang WC (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17:859–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Li M, Wang P, Cox KL Jr, Duan L, Dever JK, 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  Google Scholar 

  • Meng XZ, Xu J, He YX, Yang KY, Mordorski B, Liu YD, Zhang SQ (2013) Phosphorylation of an ERF transcriptionfactor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25:1126–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, Uhrig J, Weyhe M, Scheel D, Lee J (2014) The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of 'VQ-motif'-containing proteins to regulate immune responses. New Phytol 203:592–606

    Article  CAS  PubMed  Google Scholar 

  • Reszka AA, Seger R, Diltz CD, Krebs EG, Fischer EH (1995) Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc Natl Acad Sci USA 92:8881–8885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyna NS, Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol Plant Microbe Interact 19:530–540

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007) The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J 49:899–909

    Article  CAS  PubMed  Google Scholar 

  • Sethi V, Raghuram B, Sinha AK, Chattopadhyay S (2014) A mitogen-activated protein kinase cascade module, MKK3-MPK6 and MYC2, is involved in blue light-mediated seedling development in Arabidopsis. Plant Cell 26:3343–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, An HL, Zhang L, Gao Z, Guo XQ (2010) GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol 74:1–17

    Article  CAS  PubMed  Google Scholar 

  • Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19:805–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y (2010) HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 51:1766–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang NN, Zhao LL, Lu R, Li Y, Li XB (2015) Cotton mitogen-activated protein kinase4 (GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic Stresses. Plant Cell Tiss Organ Cult 123:619–632

    Article  CAS  Google Scholar 

  • Wang F, Wang C, Yan Y, Jia H, Guo X (2016) Overexpression of cotton GhMPK11 decreases disease resistance through the gibberellin signaling pathway in transgenic Nicotiana benthamiana. Front Plant Sci 7:689

    PubMed  PubMed Central  Google Scholar 

  • Wang M, Tu L, Yuan D, Zhu SC, Li J, Liu F, Pei L, Wang P, Zhao G, Ye Z, Huang H, Yan F, Ma Y, Zhang L, Liu M, You J, Yang Y, Liu Z, Huang F, Li B, Qiu P, Zhang Q, Zhu L, Jin S, Yang X, Min L, Li G, Chen LL, Zheng H, Lindsey K, Lin Z, Udall JA, Zhang X (2019) Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat Genet 51:224–229

    Article  CAS  PubMed  Google Scholar 

  • Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186

    Article  Google Scholar 

  • Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143–180

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Gen Genomics 280:187–198

    Article  CAS  Google Scholar 

  • Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZT, Zhou Y, Li Y, Shao SQ, Li BY, Shi HY, Li XB (2010) Interactome analysis of the six cotton 14-3-3s that are preferentially expressed in fibres and involved in cell elongation. J Exp Bot 61:3331–3344

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zou D, Li Y, Sun X, Wang NN, Li XB (2014a) GhMPK17, a cotton mitogen-activated protein kinase, is involved in plant response to high salinity and osmotic stresses and ABA signaling. PLoS ONE 9:e95642

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Wang L, Xu X, Cai C, Guo W (2014b) 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Wu H, Su J, Wang H, Zhu Q, Liu Y, Xu J, Lukowitz W, Zhang S (2017) Maternal control of embryogenesis by MPK6 and its upstream MKK4/MKK5 in Arabidopsis. Plant J 92:1005–1019

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Cochet F, Ponnaiah M, Lebreton S, Matheron L, Pionneau C, Boudsocq M, Resentini F, Huguet S, Blázquez MÁ, Bailly C, Puyaubert J, Baudouin E (2019) The MPK8-TCP14 pathway promotes seed germination in Arabidopsis. Plant J 100:677–692

    Article  CAS  PubMed  Google Scholar 

  • Zhao FY, Hu F, Zhang SY, Wang K, Zhang CR, Liu T (2013) MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environ Sci Pollut Res Int 20:5449–5460

    Article  CAS  PubMed  Google Scholar 

  • Zhao F, Zheng YF, Zeng T, Sun R, Yang JY, Li Y, Ren DT, Ma H, Xu ZH, Bai SN (2017) Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 kinase is required for anther development. Plant Physiol 173:2265–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Shao Y, Ge S, Zhang M, Zhang T, Hu X, Liu Y, Walker J, Zhang S, Xu J (2019) A MAPK cascade downstream of IDA-HAE/HSL2 ligand-receptor pair in lateral root emergence. Nat Plants 5:414–423

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by National Key R&D Program of China (Grant No. 2016YFD0100505), Project of Transgenic Research from the Ministry of Agriculture of China (Grant No. 2016ZX08009003-004), and National Natural Sciences Foundation of China (Grant No. 31871667).

Author information

Authors and Affiliations

Authors

Contributions

XBL conceived and designed the research; YHC, NNW, JBZ and YZ, performed the experiments; YHC, NNW and XBL analyzed data and wrote the paper.

Corresponding author

Correspondence to Xue-Bao Li.

Ethics declarations

Conflict of interest

The authors declare no any competing interests.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 312 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, YH., Wang, NN., Zhang, JB. et al. Genome-wide identification of the mitogen-activated protein kinase (MAPK) family in cotton (Gossypium hirsutum) reveals GhMPK6 involved in fiber elongation. Plant Mol Biol 103, 391–407 (2020). https://doi.org/10.1007/s11103-020-00999-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-00999-9

Keywords

Navigation