1932

Abstract

Plant mitogen-activated protein kinases (MAPKs) constitute a network of signaling cascades responsible for transducing extracellular stimuli and decoding them to dedicated cellular and developmental responses that shape the plant body. Over the last decade, we have accumulated information about how MAPK modules control the development of reproductive tissues and gametes and the embryogenic and postembryonic development of vegetative organs such as roots, root nodules, shoots, and leaves. Of key importance to understanding how MAPKs participate in developmental and environmental signaling is the characterization of their subcellular localization, their interactions with upstream signal perception mechanisms, and the means by which they target their substrates. In this review, we summarize the roles of MAPK signaling in the regulation of key plant developmental processes, and we survey what is known about the mechanisms guiding the subcellular compartmentalization of MAPK modules.

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2018-04-29
2024-06-16
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Literature Cited

  1. Abiko M, Furuta K, Yamauchi Y, Fujita C, Taoka M. 1.  et al. 2013. Identification of proteins enriched in rice egg or sperm cells by single-cell proteomics. PLOS ONE 8:e69578 [Google Scholar]
  2. Bain G, Cravatt CB, Loomans C, Alberola-Ila J, Hedrick SM, Murre C. 2.  2001. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat. Immunol. 2:165–71 [Google Scholar]
  3. Bartels S, González Besteiro MA, Lang D, Ulm R. 3.  2010. Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci 15:322–29 [Google Scholar]
  4. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. 4.  2009. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–88 [Google Scholar]
  5. Beck M, Komis G, Müller J, Menzel D, Šamaj J. 5.  2010. Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 22:755–71The first study to show the role of the ANP-MPK4 pathway in the regulation of cortical microtubule organization and dynamics. [Google Scholar]
  6. Beck M, Komis G, Ziemann A, Menzel D, Šamaj J. 6.  2011. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 189:1069–83 [Google Scholar]
  7. Bergmann DC, Lukowitz W, Somerville CR. 7.  2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–97 [Google Scholar]
  8. Bergmann DC, Sack FD. 8.  2007. Stomatal development. Annu. Rev. Plant Biol. 58:163–81 [Google Scholar]
  9. Berriri S, Garcia AV, Frei dit Frey N, Rozhon W, Pateyron S. 9.  et al. 2012. Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. Plant Cell 24:4281–93The first study to describe the preparation of constitutively active MAPKs and their biological potential. [Google Scholar]
  10. Berson T, von Wangenheim D, Takáč T, Šamajová O, Rosero A. 10.  et al. 2014. Trans-Golgi network localized small GTPase RabA1d is involved in cell plate formation and oscillatory root hair growth. BMC Plant Biol 14:252 [Google Scholar]
  11. Bögre L, Calderini O, Binarova P, Mattauch M, Till S. 11.  et al. 1999. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 11:101–13 [Google Scholar]
  12. Bush SM, Krysan PJ. 12.  2007. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J. Exp. Bot. 58:2181–91 [Google Scholar]
  13. Calderini O, Bögre L, Vicente O, Binarova P, Heberle-Bors E, Wilson C. 13.  1998. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. J. Cell Sci. 111:3091–100 [Google Scholar]
  14. Chai L, Tudor RL, Poulter NS, Wilkins KA, Eaves DJ. 14.  et al. 2017. MAP kinase PrMPK9–1 contributes to the self-incompatibility response. Plant Physiol 174:1226–37 [Google Scholar]
  15. Chao Q, Gao ZF, Wang YF, Li Z, Huang XH. 15.  et al. 2016. The proteome and phosphoproteome of maize pollen uncovers fertility candidate proteins. Plant Mol. Biol. 91:287–304 [Google Scholar]
  16. Chen J, Zhang Q, Wang Q, Feng M, Li Y. 16.  et al. 2017. RhMKK9, a rose MAP KINASE KINASE gene, is involved in rehydration-triggered ethylene production in rose gynoecia. BMC Plant Biol 17:51 [Google Scholar]
  17. Chen L, Chen Q, Zhu Y, Hou L, Mao P. 17.  2016. Proteomic identification of differentially expressed proteins during alfalfa (Medicago sativa L.) flower development. Front. Plant Sci. 7:1502 [Google Scholar]
  18. Chen T, Zhou B, Duan L, Zhu H, Zhang Z. 18.  2017. MtMAPKK4 is an essential gene for growth and reproduction of Medicago truncatula. Physiol. Plant 159:492–503 [Google Scholar]
  19. Chen T, Zhu H, Ke D, Cai K, Wang C. 19.  et al. 2012. A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24:823–38 [Google Scholar]
  20. Cheng Z, Li JF, Niu Y, Zhang XC, Woody OZ. 20.  et al. 2015. Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521:213–16Elucidates how RACK1 proteins act as scaffolds for MAPK signaling. [Google Scholar]
  21. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL. 21.  et al. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. PNAS 105:15629–34 [Google Scholar]
  22. Choi KY, Satterberg B, Lyons DM, Elion EA. 22.  1994. Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78:499–512 [Google Scholar]
  23. Conlon P, Gelin-Licht R, Ganesan A, Zhang J, Levchenko A. 23.  2016. Single-cell dynamics and variability of MAPK activity in a yeast differentiation pathway. PNAS 113:E5896–905 [Google Scholar]
  24. Coronado MJ, González-Melendi P, Seguí JM, Ramírez C, Bárány I. 24.  et al. 2002. MAPKs entry into the nucleus at specific interchromatin domains in plant differentiation and proliferation processes. J. Struct. Biol. 140:200–13 [Google Scholar]
  25. Coronado MJ, Testillano PS, Wilson C, Vicente O, Heberle-Bors E, Risueño MC. 25.  2007. In situ molecular identification of the Ntf4 MAPK expression sites in maturing and germinating pollen. Biol. Cell 99:209–21 [Google Scholar]
  26. Demeautis C, Sipieter F, Roul J, Chapuis C, Padilla-Parra S. 26.  et al. 2017. Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM. Sci. Rep. 7:41026 [Google Scholar]
  27. Dhanasekaran DN, Kashef K, Lee CM, Xu H, Reddy EP. 27.  2007. Scaffold proteins of MAP-kinase modules. Oncogene 26:3185–202 [Google Scholar]
  28. Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H. 28.  2007. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318:453–56 [Google Scholar]
  29. Dong J, MacAlister CA, Bergmann DC. 29.  2009. BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–30 [Google Scholar]
  30. Duan P, Rao Y, Zeng D, Yang Y, Xu R. 30.  et al. 2014. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J 77:547–57 [Google Scholar]
  31. Fernandez-Pascual M, Lucas MM, de Felipe MR, Boscá L, Hirt H, Golvano MP. 31.  2006. Involvement of mitogen-activated protein kinases in the symbiosis BradyrhizobiumLupinus. J. Exp. Bot 57:2735–42 [Google Scholar]
  32. Forde BG, Cutler SR, Zaman N, Krysan PJ. 32.  2013. Glutamate signalling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture. Plant J 75:1–10 [Google Scholar]
  33. Gao M, Liu J, Bi D, Zhang Z, Cheng F. 33.  et al. 2008. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–98 [Google Scholar]
  34. Genot B, Lang J, Berriri S, Garmier M, Gilard F. 34.  et al. 2017. Constitutively active Arabidopsis MAP kinase 3 triggers defense responses involving salicylic acid and SUMM2 resistance protein. Plant Physiol 174:1238–49 [Google Scholar]
  35. Guan Y, Lu J, Xu J, McClure B, Zhang S. 35.  2014. Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol 165:528–33 [Google Scholar]
  36. Guan Y, Meng X, Khanna R, LaMontagne E, Liu Y, Zhang S. 36.  2014. Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLOS Genet 10:e1004384 [Google Scholar]
  37. Gudesblat GE, Schneider-Pizoń J, Betti C, Mayerhofer J, Vanhoutte I. 37.  et al. 2012. SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell Biol. 14:548–54Shows the redundant regulation of SPEECHLESS by MAPKs and GSKs. [Google Scholar]
  38. Guo H, Feng P, Chi W, Sun X, Xu X. 38.  et al. 2016. Plastid-nucleus communication involves calcium-modulated MAPK signalling. Nat. Commun. 7:12173 [Google Scholar]
  39. Guo J, Chen JG. 39.  2008. RACK1 genes regulate plant development with unequal genetic redundancy in Arabidopsis. BMC Plant Biol 8:108 [Google Scholar]
  40. Guo J, Wang S, Wang J, Huang WD, Liang J, Chen JG. 40.  2009. Dissection of the relationship between RACK1 and heterotrimeric G-proteins in Arabidopsis. Plant Cell Physiol 50:1681–94 [Google Scholar]
  41. Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M. 41.  et al. 2006. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–98 [Google Scholar]
  42. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S. 42.  et al. 2009. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–31 [Google Scholar]
  43. Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Röhrig H. 43.  et al. 2013. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Mol. Cell. Proteom. 12:369–80 [Google Scholar]
  44. Hord CL, Sun YJ, Pillitteri LJ, Torii KU, Wang H. 44.  et al. 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 1:645–58 [Google Scholar]
  45. Hunt L, Bailey KJ, Gray JE. 45.  2010. The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol 186:609–14 [Google Scholar]
  46. Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H. 46.  2011. Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23:1153–70 [Google Scholar]
  47. Ishikawa M, Soyano T, Nishihama R, Machida Y. 47.  2002. The NPK1 mitogen-activated protein kinase kinase kinase contains a functional nuclear localization signal at the binding site for the NACK1 kinesin-like protein. Plant J 32:789–98 [Google Scholar]
  48. Jalmi SK, Sinha AK. 48.  2016. Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice. Sci. Rep. 6:37974 [Google Scholar]
  49. Jammes F, Song C, Shin D, Munemasa S, Takeda K. 49.  et al. 2009. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. PNAS 106:20520–25 [Google Scholar]
  50. Jia W, Li B, Li S, Liang Y, Wu X. 50.  et al. 2016. Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis. PLOS Biol 14:e1002550 [Google Scholar]
  51. Johnson KL, Ramm S, Kappel C, Ward S, Leyser O. 51.  et al. 2015. The Tinkerbell (Tink) mutation identifies the dual-specificity MAPK phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) as a novel regulator of organ size in Arabidopsis. PLOS ONE 10:e0131103 [Google Scholar]
  52. Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI. 52.  et al. 2012. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. PNAS 109:19486–91 [Google Scholar]
  53. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL. 53.  et al. 2008. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20:1775–85 [Google Scholar]
  54. Kim SH, Kim HS, Bahk S, An J, Yoo Y. 54.  et al. 2017. Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res 45:6613–27 [Google Scholar]
  55. Kim TW, Michniewicz M, Bergmann DC, Wang ZY. 55.  2012. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–22 [Google Scholar]
  56. Kohoutová L, Kourová H, Nagy SK, Volc J, Halada P. 56.  et al. 2015. The Arabidopsis mitogen-activated protein kinase 6 is associated with γ-tubulin on microtubules, phosphorylates EB1c and maintains spindle orientation under nitrosative stress. New Phytol 207:1061–74 [Google Scholar]
  57. Komis G, Mistrik M, Šamajová O, Ovečka M, Bartek J, Šamaj J. 57.  2015. Superresolution live imaging of plant cells using structured illumination microscopy. Nat. Protoc. 10:1248–63 [Google Scholar]
  58. Kong X, Pan J, Zhang M, Xing X, Zhou Y. 58.  et al. 2011. ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ 34:1291–303 [Google Scholar]
  59. Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M. 59.  et al. 2010. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22:3778–90Resolves the entire pathway composed of ANPs, MKK6, and MPK4 regulating plant cytokinesis. [Google Scholar]
  60. Krysan PJ, Jester PJ, Gottwald JR, Sussman MR. 60.  2002. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell 14:1109–20 [Google Scholar]
  61. Kumar KR, Kirti PB. 61.  2010. A mitogen-activated protein kinase, AhMPK6 from peanut localizes to the nucleus and also induces defense responses upon transient expression in tobacco. Plant Physiol. Biochem. 48:481–86 [Google Scholar]
  62. Lampard GR, Lukowitz W, Ellis BE, Bergmann DC. 62.  2009. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21:3506–17Identifies MKK7 and MKK9 as regulators of stomatal ontogenesis and assigns protein localization properties to their D motifs (see also Reference 64). [Google Scholar]
  63. Lampard GR, Macalister CA, Bergmann DC. 63.  2008. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–16 [Google Scholar]
  64. Lampard GR, Wengier DL, Bergmann DC. 64.  2014. Manipulation of mitogen-activated protein kinase kinase signaling in the Arabidopsis stomatal lineage reveals motifs that contribute to protein localization and signaling specificity. Plant Cell 26:3358–71Identifies MKK7 and MKK9 as regulators of stomatal ontogenesis and assigns protein localization properties to their D motifs (see also Reference 62). [Google Scholar]
  65. Lazar A, Coll A, Dobnik D, Baebler Š, Bedina-Zavec A. 65.  et al. 2014. Involvement of potato (Solanum tuberosum L.) MKK6 in response to Potato virus Y. PLOS ONE 9:e104553 [Google Scholar]
  66. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM. 66.  et al. 2012. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26:126–36 [Google Scholar]
  67. Lee Y, Kim YJ, Kim MH, Kwak JM. 67.  2016. MAPK cascades in guard cell signal transduction. Front. Plant Sci. 7:80 [Google Scholar]
  68. Li S, Šamaj J, Franklin-Tong VE. 68.  2007. A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility in Papaver pollen. Plant Physiol 145:236–45 [Google Scholar]
  69. Li Y, Zhang L, Wang X, Zhang W, Hao L. 69.  et al. 2013. Cotton GhMPK6a negatively regulates osmotic tolerance and bacterial infection in transgenic Nicotiana benthamiana, and plays a pivotal role in development. FEBS J 280:5128–44 [Google Scholar]
  70. Ligterink W, Kroj T, zur Nieden U, Hirt H, Scheel D. 70.  1997. Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276:2054–57 [Google Scholar]
  71. Limmongkon A, Giuliani C, Valenta R, Mittermann I, Heberle-Bors E, Wilson C. 71.  2004. MAP kinase phosphorylation of plant profilin. Biochem. Biophys. Res. Commun. 324:382–86 [Google Scholar]
  72. Liu JY, Horstman HD, Braun E, Graham MA, Zhang C. 72.  et al. 2011. Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol 157:1363–78 [Google Scholar]
  73. Liu S, Hua L, Dong S, Chen H, Zhu X. 73.  2015. OsMAPK6, a mitogen-activated protein kinase, influences rice grain size and biomass production. Plant J 84:672–81 [Google Scholar]
  74. López-Bucio JS, Dubrovsky JG, Raya-González J, Ugartechea-Chirino Y, López-Bucio J. 74.  et al. 2014. Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J. Exp. Bot. 65:169–83 [Google Scholar]
  75. Lu W, Chu X, Li Y, Wang C, Guo X. 75.  2013. Cotton GhMKK1 induces the tolerance of salt and drought stress, and mediates defence responses to pathogen infection in transgenic Nicotiana benthamiana. PLOS ONE 8:e68503 [Google Scholar]
  76. Lukowitz W, Roeder A, Parmenter D, Somerville C. 76.  2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116:109–19 [Google Scholar]
  77. MacAlister CA, Ohashi-Ito K, Bergmann DC. 77.  2007. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–40 [Google Scholar]
  78. 78. MAPK Group 2002. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–8 [Google Scholar]
  79. Matsuoka D, Yasufuku T, Furuya T, Nanmori T. 79.  2015. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol. Biol. 87:565–75 [Google Scholar]
  80. Meng X, Wang H, He Y, Liu Y, Walker JC. 80.  et al. 2012. A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24:4948–60 [Google Scholar]
  81. Mitula F, Tajdel M, Cieśla A, Kasprowicz-Maluśki A, Kulik A. 81.  et al. 2015. Arabidopsis ABA-activated kinase MAPKKK18 is regulated by protein phosphatase 2C ABI1 and the ubiquitin-proteasome pathway. Plant Cell Physiol 56:2351–67 [Google Scholar]
  82. Mohanta TK, Mohanta N, Parida P, Panda SK, Ponpandian LN. 82.  2016. Genome-wide identification of mitogen-activated protein kinase gene family across fungal lineage shows presence of novel and diverse activation loop motifs. PLOS ONE 11:e0149861 [Google Scholar]
  83. Müller J, Beck M, Mettbach U, Komis G, Hause G. 83.  et al. 2010. Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J 61:234–48 [Google Scholar]
  84. Müller J, Ory S, Copeland T, Piwnica-Worms H, Morrison DK. 84.  2001. C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8:983–93 [Google Scholar]
  85. Nagy SK, Darula Z, Kállai BM, Bögre L, Bánhegyi G. 85.  et al. 2015. Activation of AtMPK9 through autophosphorylation that makes it independent of the canonical MAPK cascades. Biochem. J. 467:167–75 [Google Scholar]
  86. Negi J, Hashimoto-Sugimoto M, Kusumi K, Iba K. 86.  2014. New approaches to the biology of stomatal guard cells. Plant Cell Physiol 55:241–50 [Google Scholar]
  87. Nguyen XC, Hoang MH, Kim HS, Lee K, Liu XM. 87.  et al. 2012. Phosphorylation of the transcriptional regulator MYB44 by mitogen activated protein kinase regulates Arabidopsis seed germination. Biochem. Biophys. Res. Commun. 423:703–8 [Google Scholar]
  88. Ning J, Zhang B, Wang N, Zhou Y, Xiong L. 88.  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 23:4334–47 [Google Scholar]
  89. Nishihama R, Ishikawa M, Araki S, Soyano T, Asada T, Machida Y. 89.  2001. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev 15:352–63 [Google Scholar]
  90. Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H. 90.  et al. 2002. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109:87–99 [Google Scholar]
  91. Nishimura A, Yamamoto K, Oyama M, Kozuka-Hata H, Saito H, Tatebayashi K. 91.  2016. Scaffold protein Ahk1, which associates with Hkr1, Sho1, Ste11, and Pbs2, inhibits cross talk signaling from the Hkr1 osmosensor to the Kss1 mitogen-activated protein kinase. Mol. Cell. Biol. 36:1109–23 [Google Scholar]
  92. Novák D, Kuchařová A, Ovečka M, Komis G, Šamaj J. 92.  2016. Developmental nuclear localization and quantification of GFP-tagged EB1c in Arabidopsis root using light-sheet microscopy. Front. Plant Sci. 6:1187 [Google Scholar]
  93. Ohashi-Ito K, Bergmann DC. 93.  2006. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–505 [Google Scholar]
  94. Ovečka M, Takáč T, Komis G, Vadovič P, Bekešová S. 94.  et al. 2014. Salt-induced subcellular kinase relocation and seeding susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis. J. Exp. Bot 65:2335–50 [Google Scholar]
  95. Ovečka M, Vaškebová L, Komis G, Luptovčiak I, Smertenko A, Šamaj J. 95.  2015. Preparation of plants for developmental and cellular imaging by light-sheet microscopy. Nat. Protoc. 10:1234–47 [Google Scholar]
  96. Patharkar OR, Walker JC. 96.  2016. Core mechanisms regulating developmentally timed and environmentally triggered abscission. Plant Physiol 172:510–20 [Google Scholar]
  97. Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K. 97.  et al. 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 [Google Scholar]
  98. Persak H, Pitzschke A. 98.  2013. Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signalling. PLOS ONE 8:e57547 [Google Scholar]
  99. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU. 99.  2007. Termination of asymmetric cell division and differentiation of stomata. Nature 445:501–5 [Google Scholar]
  100. Pitzschke A.100.  2015. Modes of MAPK substrate recognition and control. Trends Plant Sci 20:49–55 [Google Scholar]
  101. Pitzschke A, Datta S, Persak H. 101.  2014. Salt stress in Arabidopsis: lipid transfer protein AZI1 and its control by mitogen-activated protein kinase MPK3. Mol. Plant 7:722–38 [Google Scholar]
  102. Plotnikov A, Zehorai E, Procaccia S, Seger R. 102.  2011. The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim. Biophys. Acta 1813:1619–33 [Google Scholar]
  103. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M. 103.  et al. 2009. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23:80–92 [Google Scholar]
  104. Posas F, Saito H. 104.  1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702–5 [Google Scholar]
  105. Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA. 105.  et al. 2012. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338:390–93 [Google Scholar]
  106. Ran JH, Shen TT, Liu WJ, Wang XQ. 106.  2013. Evolution of the bHLH genes involved in stomatal development: implications for the expansion of developmental complexity of stomata in land plants. PLOS ONE 8:e78997 [Google Scholar]
  107. Ryu H, Laffont C, Frugier F, Hwang I. 107.  2017. MAP kinase-mediated negative regulation of symbiotic nodule formation in Medicago truncatula. Mol. Cells 40:17–23 [Google Scholar]
  108. Šamaj J, Ovečka M, Hlavačka A, Lecourieux F, Meskiene I. 108.  et al. 2002. Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J 21:3296–306 [Google Scholar]
  109. Šamajová O, Komis G, Šamaj J. 109.  2014. Immunofluorescent localization of MAPKs and colocalization with microtubules in Arabidopsis seedling whole-mount probes. Methods Mol. Biol. 1171:107–15 [Google Scholar]
  110. Sasabe M, Boudolf V, De Veylder L, Inzé D, Genschik P, Machida Y. 110.  2011. Phosphorylation of a mitotic kinesin-like protein and a MAPKKK by cyclin-dependent kinases (CDKs) is involved in the transition to cytokinesis in plants. PNAS 108:17844–49 [Google Scholar]
  111. Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y. 111.  2011. Arabidopsis thaliana MAP65–1 and MAP65–2 function redundantly with MAP65–3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal. Behav. 6:743–47 [Google Scholar]
  112. Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H. 112.  et al. 2006. Phosphorylation of NtMAP65–1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 20:1004–14 [Google Scholar]
  113. Sheikh AH, Eschen-Lippold L, Pecher P, Hoehenwarter W, Sinha AK. 113.  et al. 2016. Regulation of WRKY46 transcription factor function by mitogen-activated protein kinases in Arabidopsis thaliana. Front. Plant Sci 7:61 [Google Scholar]
  114. Shi J, An H-L, Zhang L, Gao Z, Guo X-Q. 114.  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 [Google Scholar]
  115. Shi J, Zhang L, An H, Wu C, Guo X. 115.  2011. GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity. BMC Mol. Biol. 12:22 [Google Scholar]
  116. Singh P, Sinha AK. 116.  2016. A positive feedback loop governed by SUB1A1 interaction with MITOGEN-ACTIVATED PROTEIN KINASE3 imparts submergence tolerance in rice. Plant Cell 28:1127–43 [Google Scholar]
  117. Singh R, Lee MO, Lee JE, Choi J, Park JH, Kim EH. 117.  et al. 2012. Rice mitogen-activated protein kinase interactome analysis using the yeast two-hybrid system. Plant Physiol 160:477–87 [Google Scholar]
  118. Smékalová V, Luptovčiak I, Komis G, Šamajová O, Ovečka M. 118.  et al. 2014. Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol 203:1175–93Shows the importance of YODA and MPK6 signaling for cell division plane orientation in the plant primary root. [Google Scholar]
  119. Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M. 119.  et al. 2006. Control of the AtMAP65–1 interaction with microtubules through the cell cycle. J. Cell Sci. 119:3227–37 [Google Scholar]
  120. Sörensson C, Lenman M, Veide-Vilg J, Schopper S, Ljungdahl T. 120.  et al. 2012. Determination of primary sequence specificity of Arabidopsis MAPKs MPK3 and MPK6 leads to identification of new substrates. Biochem. J. 446:271–78 [Google Scholar]
  121. Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y. 121.  2003. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 17:1055–67 [Google Scholar]
  122. Stanko V, Giuliani C, Retzer K, Djamei A, Wahl V. 122.  et al. 2014. Timing is everything: Highly specific and transient expression of a MAP kinase determines auxin-induced leaf venation patterns in Arabidopsis. Mol. Plant 7:1637–52 [Google Scholar]
  123. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W. 123.  et al. 2008. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–17 [Google Scholar]
  124. Su J, Xu J, Zhang S. 124.  2015. RACK1, scaffolding a heterotrimeric G protein and a MAPK cascade. Trends Plant Sci 20:405–7 [Google Scholar]
  125. Su SH, Krysan PJ. 125.  2016. A double-mutant collection targeting MAP kinase related genes in Arabidopsis for studying genetic interactions. Plant J 88:867–78 [Google Scholar]
  126. Su SH, Suarez-Rodriguez MC, Krysan P. 126.  2007. Genetic interaction and phenotypic analysis of the Arabidopsis MAP kinase pathway mutations mekk1 and mpk4 suggests signaling pathway complexity. FEBS Lett 581:3171–77 [Google Scholar]
  127. Suzuki T, Matsushima C, Nishimura S, Higashiyama T, Sasabe M, Machida Y. 127.  2016. Identification of phosphoinositide-binding protein PATELLIN2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis. Plant Cell Physiol 57:1744–55 [Google Scholar]
  128. Takáč T, Vadovič P, Pechan T, Luptovčiak I, Šamajová O, Šamaj J. 128.  2016. Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6. Sci. Rep 6:28306 [Google Scholar]
  129. Takahashi F, Mizoguchi T, Yoshida R, Ichimura K, Shinozaki K. 129.  2011. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell 41:649–60 [Google Scholar]
  130. Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y. 130.  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 51:1766–76 [Google Scholar]
  131. Tanaka K, Tatebayashi K, Nishimura A, Yamamoto K, Yang HY, Saito H. 131.  2014. Yeast osmosensors Hkr1 and Msb2 activate the Hog1 MAPK cascade by different mechanisms. Sci. Signal. 7:ra21 [Google Scholar]
  132. Tanoue T, Nishida E. 132.  2003. Molecular recognitions in the MAP kinase cascades. Cell Signal 15:455–62 [Google Scholar]
  133. Teichert I, Steffens EK, Schnaß N, Fränzel B, Krisp C. 133.  et al. 2014. PRO40 is a scaffold protein of the cell wall integrity pathway, linking the MAP kinase module to the upstream activator protein kinase C. PLOS Genet 10:e1004582 [Google Scholar]
  134. Teis D, Wunderlich W, Huber LA. 134.  2002. Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3:803–14 [Google Scholar]
  135. Ueda M, Aichinger E, Gong W, Groot E, Verstraeten I. 135.  et al. 2017. Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Genes Dev 31:617–27Connects YODA signaling to the activation of WOX8 via MPK3/MPK6 phosphorylation of the WRKY2 transcription factor. [Google Scholar]
  136. Umbrasaite J, Schweighofer A, Kazanaviciute V, Magyar Z, Ayatollahi Z. 136.  et al. 2010. MAPK phosphatase AP2C3 induces ectopic proliferation of epidermal cells leading to stomata development in Arabidopsis. PLOS ONE 5:e15357 [Google Scholar]
  137. Underwood W, Melotto M, He SY. 137.  2007. Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–29 [Google Scholar]
  138. Voronin V, Aionesei T, Limmongkon A, Barinova I, Touraev A. 138.  et al. 2004. The MAP kinase kinase NtMEK2 is involved in tobacco pollen germination. FEBS Lett 560:86–90 [Google Scholar]
  139. Voronin V, Touraev A, Kieft H, van Lammeren AA, Heberle-Bors E. 139.  et al. 2001. Temporal and tissue-specific expression of the tobacco ntf4 MAP kinase. Plant Mol. Biol. 45:679–89 [Google Scholar]
  140. Walia A, Lee JS, Wasteneys G, Ellis B. 140.  2009. Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant J 59:565–75 [Google Scholar]
  141. Wang C, Wang G, Zhang C, Zhu P, Dai H. 141.  et al. 2017. OsCERK1-mediated chitin perception and immune signaling requires receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in rice. Mol. Plant 10:619–33 [Google Scholar]
  142. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. 142.  2007. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73 [Google Scholar]
  143. Wang F, Shang Y, Fan B, Yu JQ, Chen Z. 143.  2014. Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense. PLOS Pathog 10:e1004243 [Google Scholar]
  144. Winnicki K, Żabka A, Bernasińska J, Matczak K, Maszewski J. 144.  2015. Immunolocalization of dually phosphorylated MAPKs in dividing root meristem cells of Vicia faba, Pisum sativum, Lupinus luteus and Lycopersicon esculentum. Plant Cell Rep 34:905–17 [Google Scholar]
  145. Wu L, Zu X, Zhang H, Wu L, Xi Z, Chen Y. 145.  et al. 2015. Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana. Plant Mol. Biol 88:429–43 [Google Scholar]
  146. Yamada K, Yamaguchi K, Shirakawa T, Nakagami H, Mine A. 146.  et al. 2016. The Arabidopsis CERK1-associated kinase PBL27 connects chitin perception to MAPK activation. EMBO J 35:2468–83 [Google Scholar]
  147. Yamada K, Yamaguchi K, Yoshimura S, Terauchi A, Kawasaki T. 147.  2017. Conservation of chitin-induced MAPK signaling pathways in rice and Arabidopsis. Plant Cell Physiol 58:993–1002 [Google Scholar]
  148. Yanagawa Y, Yoda H, Osaki K, Amano Y, Aono M. 148.  et al. 2016. Mitogen-activated protein kinase 4-like carrying an MEY motif instead of a TXY motif is involved in ozone tolerance and regulation of stomatal closure in tobacco. J. Exp. Bot. 67:3471–79 [Google Scholar]
  149. Yi J, Lee YS, Lee DY, Cho MH, Jeon JS, An G. 149.  2016. OsMPK6 plays a critical role in cell differentiation during early embryogenesis in Oryza sativa. J. Exp. Bot 67:2425–37 [Google Scholar]
  150. Yoo S-D, Cho Y-H, Tena G, Xiong Y, Sheen J. 150.  2008. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451:789–95 [Google Scholar]
  151. Yu L, Nie J, Cao C, Jin Y, Yan M. 151.  et al. 2010. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–73 [Google Scholar]
  152. Yue H, Nie S, Xing D. 152.  2012. Over-expression of Arabidopsis Bax inhibitor-1 delays methyl jasmonate-induced leaf senescence by suppressing the activation of MAP kinase 6. J. Exp. Bot. 63:4463–74 [Google Scholar]
  153. Zaïdi I, Ebel C, Touzri M, Herzog E, Evrard JL. 153.  et al. 2010. TMKP1 is a novel wheat stress responsive MAP kinase phosphatase localized in the nucleus. Plant Mol. Biol. 73:325–38 [Google Scholar]
  154. Zeng Q, Chen JG, Ellis BE. 154.  2011. AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 67:895–906 [Google Scholar]
  155. Zeng Q, Sritubtim S, Ellis BE. 155.  2011. AtMKK6 and AtMPK13 are required for lateral root formation in Arabidopsis. Plant Signal. Behav. 6:1436–39 [Google Scholar]
  156. Zhang L, Chen XJ, Lu HB, Xie ZP, Staehelin C. 156.  2011. Functional analysis of the type 3 effector nodulation outer protein L (NopL) from Rhizobium sp. NGR234: symbiotic effects, phosphorylation, and interference with mitogen-activated protein kinase signaling. J. Biol. Chem. 286:32178–87 [Google Scholar]
  157. Zhang L, Li Y, Lu W, Meng F, Wu CA, Guo X. 157.  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 63:3935–51 [Google Scholar]
  158. Zhang X, Xu X, Yu Y, Chen C, Wang J. 158.  et al. 2016. Integration analysis of MKK and MAPK family members highlights potential MAPK signaling modules in cotton. Sci. Rep. 6:29781 [Google Scholar]
  159. Zhang Y, Bergmann DC, Dong J. 159.  2016. Fine-scale dissection of the subdomains of polarity protein BASL in stomatal asymmetric cell division. J. Exp. Bot. 67:5093–103 [Google Scholar]
  160. Zhang Y, Guo X, Dong J. 160.  2016. Phosphorylation of the polarity protein BASL differentiates asymmetric cell fate through MAPKs and SPCH. Curr. Biol. 26:2957–65 [Google Scholar]
  161. Zhang Y, Wang P, Shao W, Zhu JK, Dong J. 161.  2015. The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev. Cell 33:136–49 [Google Scholar]
  162. Zhao C, Nie H, Shen Q, Zhang S, Lukowitz W, Tang D. 162.  2014. EDR1 physically interacts with MKK4/MKK5 and negatively regulates a MAP kinase cascade to modulate plant innate immunity. PLOS Genet 10:e1004389 [Google Scholar]
  163. Zhao F, Zheng YF, Zeng T, Sun R, Yang JY. 163.  et al. 2017. Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 kinase is required for anther development. Plant Physiol 173:2265–77 [Google Scholar]
  164. Zhao P, Sokolov LN, Ye J, Tang CY, Shi J. 164.  et al. 2016. The LIKE SEX FOUR2 regulates root development by modulating reactive oxygen species homeostasis in Arabidopsis. Sci. Rep 6:28683 [Google Scholar]
  165. Zhou C, Cai Z, Guo Y, Gan S. 165.  2009. An Arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150:167–77 [Google Scholar]
  166. Zong X-J, Li D-P, Gu L-K, Li D-Q, Liu L-X, Hu X-L. 166.  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 229:485–95 [Google Scholar]
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