Skip to main content
SpringerLink
Log in

Genome‑wide identification of MPK and MKK gene families and their responses to phytohormone treatment and abiotic stress in foxtail millet

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The mitogen-activated protein kinase (MAPK) cascade is one of the most important pathways in eukaryotic signaling networks, and it plays a crucial role in plant growth and development, hormonal responses, and responses to various biotic and abiotic stress. Foxtail millet (Setaria italica) is a minor cereal with excellent nutritional value and fine adaptability to abiotic stress associated with climate change, and it has also emerged as a C4 model plant. MAPK cascade genes from several model plant species have been analyzed, but not from foxtail millet. Here, 16 SiMPKs and 11 SiMKKs were systematically identified and analyzed in foxtail millet. Phylogenetic relationships, conserved protein motifs, and gene structure indicated clearly that both MPKs and MKKs were divided into four subgroups. RNA-seq data analysis showed that expression profiles of some SiMPK and SiMKK genes varied in different tissues or developmental stages. Furthermore, the expression levels of SiMPK and SiMKK genes under abiotic stresses as well as exogenously applied phytohormone were also investigated. The identified abiotic stress and phytohormone responsive genes suggested that the SiMPKs, SiMKKs, and MKK-MPK interactomes play key roles in abiotic stress and hormone signaling pathways and networks. Our study provides detailed information of MKK and MPK genes in foxtail millet and lays the foundation to explore their functional characterization for stress-tolerance.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • 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(6875):977–983

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:202–208

    Article  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488

    Article  CAS  PubMed  Google Scholar 

  • Barton L, Newsome SD, Chen FH, Wang H, Guilderson TP, Bettinger RL (2009) Agricultural origins and the isotopic identity of domestication in northern China. Proc Natl Acad Sci U S A 106(14):5523–5528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30(6):555–561

    Article  CAS  PubMed  Google Scholar 

  • Çakır B, Kılıçkaya O (2015) Mitogen-activated protein kinase cascades in Vitis vinifera. Front Plant Sci 6:556

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13(8):1194–1202

    Article  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 (2012a) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS ONE 7(10):e46744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen T, Zhu H, Ke D, Cai K, Wang C, Gou H, Hong Z, Zhang Z (2012b) A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24(2):823–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YH, Wang NN, Zhang JB, Zheng Y, Li XB (2020b) 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(4–5):391–407

    Article  CAS  PubMed  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413(2):217–226

    Article  CAS  PubMed  Google Scholar 

  • Danquah A, de Zélicourt A, Boudsocq M, Neubauer J, Frei Dit Frey N, Leonhardt N, Pateyron S, Gwinner F, Tamby JP, Ortiz-Masia D, Marcote MJ, Hirt H, Colcombet J (2015) Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J 82(2):232–244

    Article  CAS  PubMed  Google Scholar 

  • Doust AN, Kellogg EA, Devos KM, Bennetzen JL (2009) Foxtail millet: a sequence-driven grass model system. Plant Physiol 149(1):137–141

    Article  CAS  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(11):2025–2030

    Article  CAS  PubMed  Google Scholar 

  • Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18(12):1190–1198

    Article  CAS  PubMed  Google Scholar 

  • Genot B, Lang J, Berriri S, Garmier M, Gilard F, Pateyron S, Haustraete K, Van Der Straeten D, Hirt H, Colcombet J (2017) Constitutively Active Arabidopsis MAP Kinase 3 Triggers Defense Responses Involving Salicylic Acid and SUMM2 Resistance Protein. Plant Physiol 174(2):1238–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186

    Article  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(4):192–198

    Article  CAS  PubMed  Google Scholar 

  • Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2(7):516–527

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiménez C, Cossío BR, Rivard CJ, Berl T, Capasso JM (2007) Cell division in the unicellular microalga Dunaliella viridis depends on phosphorylation of extracellular signal-regulated kinases (ERKs). J Exp Bot 58(5):1001–1011

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kong F, Wang J, Cheng L, Liu S, Wu J, Peng Z, Lu G (2012a) Genome-wide analysis of the mitogen-activated protein kinase gene family in Solanum lycopersicum. Gene 499(1):108–120

    Article  CAS  PubMed  Google Scholar 

  • Kong Q, Qu N, Gao M, Zhang Z, Ding X, Yang F, Li Y, Dong OX, Chen S, Li X, Zhang Y (2012b) The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24(5):2225–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong X, Pan J, Zhang D, Jiang S, Cai G, Wang L, Li D (2013) Identification of mitogen-activated protein kinase kinase gene family and MKK-MAPK interaction network in maize. Biochem Biophys Res Commun 441(4):964–969

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JS, Huh KW, Bhargava A, Ellis BE (2008) Comprehensive analysis of protein-protein interactions between Arabidopsis MAPKs and MAPK kinases helps define potential MAPK signalling modules. Plant Signal Behav 3(12):1037–1041

    Article  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(6):975–985

    Article  CAS  PubMed  Google Scholar 

  • Lee SK, Kim BG, Kwon TR, Jeong MJ, Park SR, Lee JW, Byun MO, Kwon HB, Matthews BF, Hong CB, Park SC (2011) Overexpression of the mitogen-activated protein kinase gene OsMAPK33 enhances sensitivity to salt stress in rice (Oryza sativa L.). J Biosci 36(1):139–151

    Article  CAS  PubMed  Google Scholar 

  • Li K, Yang F, Zhang G, Song S, Li Y, Ren D, Miao Y, Song CP (2017) AIK1, A Mitogen-Activated Protein Kinase, Modulates Abscisic Acid Responses through the MKK5-MPK6 Kinase Cascade. Plant Physiol 173(2):1391–1408

    Article  CAS  PubMed  Google Scholar 

  • Li P, Brutnell TP (2011) Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. J Exp Bot 62(9):3031–3037

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhang Y, Huang L, Ouyang Z, Hong Y, Zhang H, Li D, Song F (2014) Tomato SlMKK2 and SlMKK4 contribute to disease resistance against Botrytis cinerea. BMC Plant Biol 14:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Shi L, Liu Y, Tang Q, Shen L, Yang S, Cai J, Yu H, Wang R, Wen J, Lin Y, Hu J, Liu C, Zhang Y, Mou S, He S (2015) Genome-wide identification and transcriptional expression analysis of mitogen-activated protein kinase and mitogen-activated protein kinase kinase genes in Capsicum annuum. Front Plant Sci 6:780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka D, Soga K, Yasufuku T, Nanmori T (2018) Control of plant growth and development by overexpressing MAP3K17, an ABA-inducible MAP3K, in Arabidopsis. Plant Biotechnol (Tokyo) 35(2):171–176

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266

    Article  CAS  PubMed  Google Scholar 

  • Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A (2021) Pfam: The protein families database in 2021. Nucleic Acids Res 49:412–d419

    Article  Google Scholar 

  • Muthamilarasan M, Singh RK, Suresh BV, Rana S, Dulani P, Prasad M (2020) Genomic dissection and expression analysis of stress-responsive genes in C4 panicoid models, Setaria italica and Setaria viridis. J Biotechnol 318:57–67

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009a) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12(4):421–426

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009b) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12(4):421–426

    Article  CAS  PubMed  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23(1):80–92

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JH, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25(6):2115–2131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Jwa NS (2013) The rice MAPKK-MAPK interactome: the biological significance of MAPK components in hormone signal transduction. Plant Cell Rep 32(6):923–931

    Article  CAS  PubMed  Google Scholar 

  • Song Q, Li D, Dai Y, Liu S, Huang L, Hong Y, Zhang H, Song F (2015) Characterization, expression patterns and functional analysis of the MAPK and MAPKK genes in watermelon (Citrullus lanatus). BMC Plant Biol 15:298

    Article  PubMed  PubMed Central  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(8):1055–1067

    Article  CAS  PubMed  PubMed Central  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(1):141–152

    Article  CAS  PubMed  Google Scholar 

  • Tena G, Asai T, Chiu W-L, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4(5):392–400

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX.Curr Protoc Bioinformatics Chap.2:Unit 2.3.

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19(1):63–73

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Pan C, Wang Y, Ye L, Wu J, Chen L, Zou T, Lu G (2015) Genome-wide identification of MAPK, MAPKK, and MAPKKK gene families and transcriptional profiling analysis during development and stress response in cucumber. BMC Genomics 16(1):386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Zhao R, Li R, Yu W, Yang M, Sheng J, Shen L (2018) Enhanced drought tolerance in tomato plants by overexpression of SlMAPK1. Plant Cell, Tissue and Organ Culture (PCTOC) 133 (1):27–38

  • Wankhede DP, Misra M, Singh P, Sinha AK (2013) Rice mitogen activated protein kinase kinase and mitogen activated protein kinase interaction network revealed by in-silico docking and yeast two-hybrid approaches. PLoS ONE 8(5):e65011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552

    CAS  PubMed  Google Scholar 

  • Wilson C, Voronin V, Touraev A, Vicente O, Heberle-Bors E (1997) A developmentally regulated MAP kinase activated by hydration in tobacco pollen. Plant Cell 9(11):2093–2100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Wang J, Pan C, Guan X, Wang Y, Liu S, He Y, Chen J, Chen L, Lu G (2014) Genome-wide identification of MAPKK and MAPKKK gene families in tomato and transcriptional profiling analysis during development and stress response. PLoS ONE 9(7):e103032

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J, Zhang S (2015) Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20(1):56–64

    Article  CAS  PubMed  Google Scholar 

  • Yoo SJ, Kim SH, Kim MJ, Ryu CM, Kim YC, Cho BH, Yang KY (2014) Involvement of the OsMKK4-OsMPK1 Cascade and its Downstream Transcription Factor OsWRKY53 in the Wounding Response in Rice. Plant Pathol J 30(2):168–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Pan J, Kong X, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMKK3, a novel maize group B mitogen-activated protein kinase kinase gene, mediates osmotic stress and ABA signal responses. J Plant Physiol 169(15):1501–1510

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li Y, Xing Q, Yue L, Qi H (2020) Genome-wide identification of mitogen-activated protein kinase (MAPK) cascade and expression profiling of CmMAPKs in melon (Cucumis melo L.). PLoS ONE 15(5):e0232756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Key Research and Development Program of Shanxi Province (201903D221095) and the National Natural Science Foundation of China (31900306, 32170410).

Author information

Authors and Affiliations

  1. School of Life Science, Shanxi University, Taiyuan, Shanxi, China

    Zhen Liang, Sha Wei & Yuqing Wu

  2. Institute of Big Data Science and Industry, Shanxi University, Taiyuan, Shanxi, China

    Yingjie Guo

Authors
  1. Zhen Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sha Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingjie Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuqing Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhen Liang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Xingchun Wang.

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 Material 1

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liang, Z., Wei, S., Guo, Y. et al. Genome‑wide identification of MPK and MKK gene families and their responses to phytohormone treatment and abiotic stress in foxtail millet. Plant Growth Regul 99, 85–99 (2023). https://doi.org/10.1007/s10725-022-00877-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-022-00877-y

Keywords

Search

Navigation