Skip to main content
Log in

Expression analysis of genes encoding mitogen-activated protein kinases in maize provides a key link between abiotic stress signaling and plant reproduction

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinases (MAPKs) play important roles in stress responses and development in plants. Maize (Zea mays), an important cereal crop, is a model plant species for molecular studies. In the last decade, several MAPKs have been identified in maize; however, their functions have not been studied extensively. Genome-wide identification and expression analysis of maize MAPK genes could provide valuable information for understanding their functions. In this study, 20 non-redundant maize MAPK genes (ZmMPKs) were identified via a genome-wide survey. Phylogenetic analysis of MAPKs from maize, rice (Oryza sativa), Arabidopsis (Arabidopsis thaliana), poplar (Populus trichocarpa), and tomato (Solanum lycopersicum) classified them into four major classes. ZmMPKs in the same class had similar domains, motifs, and genomic structures. Gene duplication investigations suggested that segmental duplications made a large contribution to the expansion of ZmMPKs. A number of cis-acting elements related to plant development and response to stress and hormones were identified in the promoter regions of ZmMPKs. Furthermore, transcript profile analysis in eight tissues and organs at various developmental stages demonstrated that most ZmMPKs were preferentially expressed in reproductive tissues and organs. The transcript abundance of most ZmMPKs changed significantly under salt, drought, cold, or abscisic acid (ABA) treatments, implying that they might participate in abiotic stress and ABA signaling. These expression analyses indicated that ZmMPKs might serve as linkers between abiotic stress signaling and plant reproduction. Our data will deepen our understanding of the complexity of the maize MAPK gene family and provide new clues to investigate their functions.

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

Similar content being viewed by others

References

  • Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152

    Article  CAS  PubMed  Google Scholar 

  • Asif MH, Lakhwani D, Pathak S, Bhambhani S, Bag SK et al (2013) 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. doi:10.1007/s10142-013-0349-9

    PubMed  Google Scholar 

  • Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29

    CAS  PubMed  Google Scholar 

  • Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet 262:534–542

    Article  CAS  PubMed  Google Scholar 

  • Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA et al (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 U S A 106:8067–8072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bögre L, Calderini O, Binarova P, Mattauch M, Till S et al (1999) A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 11:101–113

    Article  PubMed Central  PubMed  Google Scholar 

  • Boudscocq M, Laurière C (2005) Osmotic signaling in plants: multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194

    Article  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Hu W, Tan S, Wang M, Ma Z et al (2012) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One 7:e46744

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Desikan R, Hancock JT, Ichimura K, Shinozaki K, Neill SJ (2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol 126:1579–1587

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Droillard MJ, Boudsocg M, Barbier-Brygoo H, Laurière C (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 574:42–48

    Article  CAS  PubMed  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 

  • Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jeong MJ, Lee SK, Kim BG et al (2006) A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell Tissue Organ Cult 85:151–160

    Article  CAS  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:162–267

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lalle M, Visconti S, Marra M, Camoni L, Velasco R et al (2005) ZmMPK6, a novel maize MAP kinase that interacts with 14-3-3 proteins. Plant Mol Biol 59:713–722

    Article  CAS  PubMed  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 

  • Long L, Gao W, Xu L, Liu M, Luo X et al (2014) GbMPK3, a mitogen-activated protein kinase from cotton, enhances drought and oxidative stress tolerance in tobacco. Plant Cell Tissue Organ Cult 116:153–162

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K et al (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 U S A 93:765–769

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mockaitis K, Howell SH (2000) Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J 24:785–796

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704

    Article  CAS  PubMed  Google Scholar 

  • Neupane A, Nepal MP, Piya S, Subramanian S, Rohila JS et al (2013) Identification, nomenclature, and evolutionary relationships of mitogen-activated protein kinase (MAPK) genes in soybean. Evol Bioinformatics Online 9:363–386

    Google Scholar 

  • Nicole MC, Hamel LP, Morency MJ, Beaudoin N, Ellis BE et al (2006) MAP-ping genomic organization and organ-specific expression profiles of poplar MAP kinases and MAP kinase kinases. BMC Genomics 7:223

    Article  PubMed Central  PubMed  Google Scholar 

  • Pan J, Zhang M, Kong X, Xing X, Liu Y et al (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235:661–676

    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 

  • Rohila JS, Yang Y (2007) Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Biol 49:751–759

    Article  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T et al (2002) Monitoring the expression pattern of around 7000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291

    Article  CAS  PubMed  Google Scholar 

  • Seo S, Seto H, Koshino H, Yoshida S, Ohashi Y (2003) A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco. Plant Cell 15:863–873

    Article  CAS  PubMed Central  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 

  • Shen QJ, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen QJ, Zhang P, Ho TH (1996) Modular nature of response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8:1107–1119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 19:63–73

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang H, Liu Y, Bruffett K, Lee J, Hause G et al (2008) Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20:602–613

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang J, Ding H, Zhang A, Ma F, Cao J et al (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wei F, Coe E, Nelson W, Bharti AK, Engler F et al (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:1254–1263

    Article  CAS  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 9:2093–2100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu T, Kong XP, Zong XJ, Li DP, Li DQ (2011) Expression analysis of five maize MAP kinase genes in response to various abiotic stresses and signal molecules. Mol Biol Rep 38:3967–3975

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Li Y, Wang Y, Liu H, Lei L et al (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 

  • Xu XH, Chen H, Sang YL, Wang F, Ma JP et al (2012) Identification of genes specifically or preferentially expressed in maize silk reveals similarity and diversity in transcript abundance of different dry stigmas. BMC Genomics 13:294

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    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 Genet Genomics 280:187–198

    Article  CAS  PubMed  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 Central  PubMed  Google Scholar 

  • Zhang A, Zhang J, Ye N, Cao J, Tan M et al (2010) ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroid-induced antioxidant defence in leaves of maize. J Exp Bot 61:4399–4411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Xu R, Luo X, Jiang Z, Shu H (2013) Genome-wide identification and expression analysis of MAPK and MAPKK gene family in Malus domestica. Gene 531:377–387

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Cai Z, Guo Y, Gan S (2009) An Arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150:167–177

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (31300266) and the Genetically Modified Organisms Breeding Major Projects (Grant No.2013ZX08003-002).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xing Bo Lu or Xiao Hui Xu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Sequence alignment and distribution of the 11 subdomains of ZmMPKs. Open and shaded areas represent unconserved and conserved regions of ZmMPKs, respectively. The degree of shading indicates the level of conservation. (GIF 463 kb)

High Resolution Image (TIFF 39125 kb)

Supplementary Fig. S2

Phylogenetic analysis of MAPK proteins in maize, rice, Arabidopsis, poplar and tomato. Numbers on the nodes are bootstrap values based on 1000 replicates. Zm, maize; Os, rice; At, Arabidopsis; Pt, poplar; Sl, tomato. (GIF 51 kb)

High Resolution Image (TIFF 2918 kb)

Supplementary Fig. S3

Slight changes in the ATP-binding domain and MAP kinase signature of ZmMPK1. The changed amino acids are marked in red. (GIF 17 kb)

High Resolution Image (TIFF 444 kb)

Supplementary Table S1

(DOC 47 kb)

Supplementary Table S2

Conserved motif sequences identified by MEME tools. The motifs were numbered in order of their statistical significance (e-value), from low to high. Width, the width of the motif; Sites, the number of sites contributing to the construction of the motif; LLR, the likelihood ratio of the motif; E-value, the statistical significance of the motif. (XLS 256 kb)

Supplementary Table S3

(DOC 49 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, W., Chen, H., Wang, J. et al. Expression analysis of genes encoding mitogen-activated protein kinases in maize provides a key link between abiotic stress signaling and plant reproduction. Funct Integr Genomics 15, 107–120 (2015). https://doi.org/10.1007/s10142-014-0410-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-014-0410-3

Keywords

Navigation