Abstract
Mitogen-activated protein kinase (MAPK) cascades are universal signal transduction modules in plants. As the last component of the MAPK cascade (MAPKKK–MAPKK–MAPK), MAPK plays important roles in linking upstream kinases and downstream substrates. The MAPK proteins belong to a complex gene family in plants, with 20 MAPK genes in the Arabidopsis genome, 17 in the rice genome, and 21 in the poplar genome. Although the maize genome sequencing has been completed, no comprehensive study has been reported thus far for the MAPK gene family in maize. In this study, we identified 19 MAPK genes in maize. These ZmMPK genes belong to four groups (A–D) found in other plants. The phylogeny, chromosomal location, gene structure, and the functional relevancy of ZmMPK genes were analyzed. Moreover, we discuss the evolutionary divergence of MAPK genes in maize. Furthermore, we analyzed the expression profiles of ZmMPKs using the public microarray data and performed expression analyses in maize seedlings and adult plants. The data obtained from our study contribute to a better understanding of the complexity of MAPKs in plants and provide a useful reference for further functional analysis of MAPK genes in maize.
Similar content being viewed by others
References
Agrawal GK, Iwahashi H, Rakwal R (2003) Rice MAPKs. Biochem Biophys Res Commun 302:171–180
Ahn S, Tanksley SD (1993) Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci USA 90:7980–7984
Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194
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
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373
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
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Chen Z, Gibson TB, Robinson F, Silvestro L, Pearson G, Xu B, Wright A, Vanderbilt C, Cobb MH (2001) MAP kinases. Chem Rev 101:2449–2476
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
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190
Ding H, Zhang A, Wang J, Lu R, Zhang H, Zhang J, Jiang M (2009) Identity of an ABA-activated 46 kDa mitogen-activated protein kinase from Zea mays leaves: partial purification, identification and characterization. Planta 230:239–251
Ding Y, Cao J, Ni L, Zhu Y, Zhang A, Tan M, Jiang M (2013) ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signalling in maize. J Exp Bot 64:871–884
Du D, Hao R, Cheng T, Pan H, Yang W, Wang J, Zhang Q (2013) Genome-Wide Analysis of the AP2/ERF Gene Family in Prunus mume. Plant Mol Biol Rep 31:741–750
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 18:1190–1198
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:D1178–D1186
Gu L, Liu Y, Zong X, Liu L, Li DP, Li DQ (2010) Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 37:4067–4073
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
Heinrich M, Baldwin IT, Wu J (2012) Three MAPK Kinases, MEK1, SIPKK, and NPK2, are not Involved in Activation of SIPK after Wounding and Herbivore Feeding but Important for Accumulation of Trypsin Proteinase Inhibitors. Plant Mol Biol Rep 30:731–740
Holland PM, Cooper JA (1999) Protein modification: docking sites for kinases. Curr Biol 9:R329–R331
Hord CL, Sun YJ, Pillitteri LJ, Torii KU, Wang H, Zhang S, Ma H (2008) Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol Plant 1:645–658
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
Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, Yamane H, Miyao A, Takatsuji H, Takahashi A, Hirochika H (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63:599–612
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 499:108–120
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 24:2225–2236
Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, Takahashi Y, Hirt H, Machida Y (2010) The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22:3778–3790
Kumar S, Stecher G, Peterson D, Tamura K (2012) MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics 28:2685–2686
Lalle M, Visconti S, Marra M, Camoni L, Velasco R, Aducci P (2005) ZmMPK6, a novel maize MAP kinase that interacts with 14-3-3 proteins. Plant Mol Biol 59:713–722
Lampard GR, Lukowitz W, Ellis BE, Bergmann DC (2009) Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21:3506–3517
Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144
Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238
Liu Y (2012) Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep 31:1–12
Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399
Liu Y, Zhou Y, Liu L, Sun L, Li D (2011) In Silico Identification and Evolutionary Analysis of Plant MAPKK6s. Plant Mol Biol Rep 29:859–865
Liu Y, Zhou Y, Liu L, Sun L, Zhang M, Liu Y, Li D (2012) Maize ZmMEK1 is a single-copy gene. Mol Biol Rep 39:2957–2966
Liu Y, Wang L, Zhang D, Li D (2013) Expression analysis of segmentally duplicated ZmMPK3-1 and ZmMPK3-2 genes in maize. Plant Mol Biol Rep 31:457–463
Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102:5454–5459
MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308
Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229
Meng X, Wang H, He Y, Liu Y, Walker JC, Torii KU, Zhang S (2012) A MAPK Cascade Downstream of ERECTA Receptor-Like Protein Kinase Regulates Arabidopsis Inflorescence Architecture by Promoting Localized Cell Proliferation. Plant Cell 24:4948–4960
Nicole MC, Hamel LP, Morency MJ, Beaudoin N, Ellis BE, Seguin A (2006) MAP-ping genomic organization and organ-specific expression profiles of poplar MAP kinases and MAP kinase kinases. BMC Genomics 7:223
Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2012) Mitogen-Activated Protein (MAP) Kinases in Plant Metal Stress: Regulation and Responses in Comparison to Other Biotic and Abiotic Stresses. Int J Mol Sci 13:7828–7853
Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235:661–676
Park YS, Kunze S, Ni X, Feussner I, Kolomiets MV (2010) Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231:1425–1437
Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120
Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3:827–837
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221
Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, Zhang S (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105:5638–5643
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
Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649
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
Samajova O, Plihal O, Al-Yousif M, Hirt H, Samaj J (2013) Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol Adv 31:118–128
Sharp PA (1981) Speculations on RNA splicing. Cell 23:643–646
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
Tanoue T, Nishida E (2003) Molecular recognitions in the MAP kinase cascades. Cell Signal 15:455–462
Tanoue T, Adachi M, Moriguchi T, Nishida E (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol 2:110–116
Teige M, Scheikl E, Eulgem T, Doczi 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
Wang H, Liu Y, Bruffett K, Lee J, Hause G, Walker JC, Zhang S (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
Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M (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
Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, Fuks G, Sanchez-Villeda H, Schroeder S, Fang Z, McMullen M, Davis G, Bowers JE, Paterson AH, Schaeffer M, Gardiner J, Cone K, Messing J, Soderlund C, Wing RA (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:e123
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
Xie G, Kato H, Imai R (2012) Biochemical identification of the OsMKK6-OsMPK3 signalling pathway for chilling stress tolerance in rice. Biochem J 443:95–102
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
Yan D-H, Xia X, Yin W (2013) NF-YB Family Genes Identified in a Poplar Genome-wide Analysis and Expressed in Populus euphratica Are Responsive to Drought Stress. Plant Mol Biol Rep 31:363–370
Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li R, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X, Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GK, Yang H (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38
Zeng Q, Chen JG, Ellis BE (2011) AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 67:895–906
Zhang A, Zhang J, Ye N, Cao J, Tan M, Zhang J, Jiang M (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
Zhou Y, Zhang D, Pan J, Kong X, Liu Y, Sun L, Wang L, Li D (2012) Overexpression of a multiple stress-responsive gene, ZmMPK4, enhances tolerance to low temperature in transgenic tobacco. Plant Physiol Biochem 58:174–181
Zong XJ, Li DP, Gu LK, Li DQ, Liu LX, Hu XL (2009) Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229:485–495
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Nos.30871457, 31071337, 31271633), the State Key Basic Research and Development Plan of China (No.2009CB118500) and the Scientific Research Foundation of Southwest Forestry University (No. 111169). The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 799 kb)
Rights and permissions
About this article
Cite this article
Liu, Y., Zhang, D., Wang, L. et al. Genome-Wide Analysis of Mitogen-Activated Protein Kinase Gene Family in Maize. Plant Mol Biol Rep 31, 1446–1460 (2013). https://doi.org/10.1007/s11105-013-0623-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-013-0623-y