AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis

Plant Journal

Volumn 67, Issue 5, 2011, Pages 895-906

  Zeng, Qingning ^a,b   Chen, Jin Gui ^a   Ellis, Brian E ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Arabidopsis; AtMKK6; AtMPK4; MAP kinase cascade; meiotic cytokinesis; pollen formation

Indexed keywords

ARABIDOPSIS; ATMKK6; ATMPK4; MAP KINASE CASCADE; MEIOTIC CYTOKINESIS; POLLEN FORMATION;

ENZYMES; GENES; PHOSPHORYLATION; PROTEINS; TISSUE;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; ATMPK4 PROTEIN, ARABIDOPSIS; COMPLEMENTARY DNA; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; PLANT RNA;

ARABIDOPSIS; ARTICLE; CYTOKINESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; MEIOSIS; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; POLLEN; PROMOTER REGION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TWO HYBRID SYSTEM; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOKINESIS; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, PLANT; MAP KINASE KINASE 6; MAP KINASE SIGNALING SYSTEM; MEIOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; POLLEN; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; RNA, PLANT; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS;

EID: 80052260693     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04642.x     Document Type: Article

References (68)

1. Alexander, M.P., (1969) Differential staining of aborted and nonaborted pollen. Stain Technol. 44, 117-122.
2. Andreasson, E., Jenkins, T., Brodersen, P., et al. (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24, 2579-2589. (Pubitemid 41076314)
3. Balasubramanian, M.K., Bi, E., and, Glotzer, M., (2004) Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14, R806-R818. (Pubitemid 39239356)
4. Beck, M., Komis, G., Muller, J., Menzel, D., and, Samaj, J., (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, 755-771.
5. Beck, M., Komis, G., Ziemann, A., Menzel, D., and, Samaj, J., (2011) Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol. 189, 1069-1083.
6. Besser, K.v., Frank, A.C., Johnson, M.A., and, Preuss, D., (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development, 133, 4761-4769. (Pubitemid 46063088)
7. Bögre, L., Calderini, O., Binarova, P., 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.
8. Brodersen, P., Petersen, M., Bjorn Nielsen, H., Zhu, S., Newman, M.A., Shokat, K.M., Rietz, S., Parker, J., and, Mundy, J., (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47, 532-546. (Pubitemid 44141699)
9. Brownfield, L., Hafidh, S., Durbarry, A., Khatab, H., Sidorova, A., Doerner, P., and, Twell, D., (2009) Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell, 21, 1940-1956.
10. Calderini, O., Glab, N., Bergounioux, C., Heberle-Bors, E., and, Wilson, C., (2001) A novel tobacco mitogen-activated protein (MAP) kinase kinase, NtMEK1, activates the cell cycle-regulated p43Ntf6 MAP kinase. J. Biol. Chem. 276, 18139-18145.
11. Canales, C., Bhatt, A.M., Scott, R., and, Dickinson, H., (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12, 1718-1727. (Pubitemid 35169787)
12. Chaiwongsar, S., Otegui, M.S., Jester, P.J., Monson, S.S., and, Krysan, P.J., (2006) The protein kinase genes MAP3K epsilon 1 and MAP3K epsilon 2 are required for pollen viability in Arabidopsis thaliana. Plant J. 48, 193-205. (Pubitemid 44484861)
13. Clark, K.A., and, Krysan, P.J., (2010) Chromosomal translocations are a common phenomenon in Arabidopsis thaliana T-DNA insertion lines. Plant J. 64, 990-1001.
14. Durbarry, A., Vizir, I., and, Twell, D., (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol. 137, 297-307. (Pubitemid 43034311)
15. Enns, L.C., Kanaoka, M.M., Torii, K.U., Comai, L., Okada, K., and, Cleland, R.E., (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol. Biol. 58, 333-349. (Pubitemid 41125991)
16. Feys, B., Benedetti, C.E., Penfold, C.N., and, Turner, J.G., (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 6, 751-759.
17. Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S., and, 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.
18. Hord, C.L., Sun, Y.J., Pillitteri, L.J., Torii, K.U., Wang, H., Zhang, S., and, 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.
19. Hulskamp, M., Parekh, N.S., Grini, P., Schneitz, K., Zimmermann, I., Lolle, S.J., and, Pruitt, R.E., (1997) The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev. Biol. 187, 114-124. (Pubitemid 27359430)
20. Ichimura, K., Mizoguchi, T., Irie, K., Morris, P., Giraudat, J., Matsumoto, K., and, Shinozaki, K., (1998) Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem. Biophys. Res. Commun. 253, 532-543. (Pubitemid 29026736)
21. Ichimura, K., Casais, C., Peck, S.C., Shinozaki, K., and, Shirasu, K., (2006) MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J. Biol. Chem. 281, 36969-36976. (Pubitemid 46042166)
22. Ishikawa, M., Soyano, T., Nishihama, R., and, Machida, Y., (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, 789-798. (Pubitemid 36010881)
23. Jouannic, S., Hamal, A., Leprince, A.S., Tregear, J.W., Kreis, M., and, Henry, Y., (1999) Plant MAP kinase kinase kinases structure, classification and evolution. Gene, 233, 1-11. (Pubitemid 29353218)
24. Jürgens, G., (2005) Cytokinesis in higher plants. Annu. Rev. Plant Biol. 56, 281-299. (Pubitemid 40802411)
25. Kaneda, M., Rensing, K.H., Wong, J.C., Banno, B., Mansfield, S.D., and, Samuels, A.L., (2008) Tracking monolignols during wood development in lodgepole pine. Plant Physiol. 147, 1750-1760. (Pubitemid 352844218)
26. Kosetsu, K., Matsunaga, S., Nakagami, H., Colcombet, J., Sasabe, M., Soyano, T., Takahashi, Y., Hirt, H., and, Machida, Y., (2010) The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell, 22, 3778-3790.
27. Krysan, P.J., Jester, P.J., Gottwald, J.R., and, Sussman, M.R., (2002) An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell, 14, 1109-1120. (Pubitemid 34616874)
28. Lee, J.S., Huh, K.W., Bhargava, A., and, Ellis, B.E., (2008) Comprehensive analysis of protein-protein interactions between Arabidopsis MAPKs and MAPK kinases helps define potential MAPK signalling modules. Plant Signal. Behav. 3, 1037-1041. (Pubitemid 352847658)
29. Li, X., Clarke, J.D., Zhang, Y., and, Dong, X., (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant Microbe Interact. 14, 1131-1139. (Pubitemid 32965026)
30. Lin, W.-Y., Matsuoka, D., Sasayama, D., and, Nanmori, T., (2010) A splice variant of Arabidopsis mitogen-activated protein kinase and its regulatory function in the MKK6-MPK13 pathway. Plant Sci. 178, 245-250.
31. Ma, H., (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393-434. (Pubitemid 40802416)
32. Melikant, B., Giuliani, C., Halbmayer-Watzina, S., Limmongkon, A., Heberle-Bors, E., and, Wilson, C., (2004) The Arabidopsis thaliana MEK AtMKK6 activates the MAP kinase AtMPK13. FEBS Lett. 576, 5-8. (Pubitemid 39330447)
33. Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V., and, Hirt, H., (2006) A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697-38704. (Pubitemid 46041996)
34. Nakashima, M., Hirano, K., Nakashima, S., Banno, H., Nishihama, R., and, Machida, Y., (1998) The expression pattern of the gene for NPK1 protein kinase related to mitogen-activated protein kinase kinase kinase (MAPKKK) in a tobacco plant: correlation with cell proliferation. Plant Cell Physiol. 39, 690-700. (Pubitemid 28348835)
35. Nishihama, R., and, Machida, Y., (2000) The MAP kinase cascade that includes MAPKKK-related protein kinase NPK1 controls a mitotic proces in plant cells. Results Probl. Cell Differ. 27, 119-130.
36. Nishihama, R., and, Machida, Y., (2001) Expansion of the phragmoplast during plant cytokinesis: a MAPK pathway may MAP it out. Curr. Opin. Plant Biol. 4, 507-512. (Pubitemid 33001800)
37. Nishihama, R., Ishikawa, M., Araki, S., Soyano, T., Asada, T., and, Machida, Y., (2001) The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev. 15, 352-363. (Pubitemid 32155150)
38. O'Brien, T.P., Feder, N., and, McCully, M.E., (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma, 59, 368-373.
39. Oh, S.A., Bourdon, V., Das 'pal, M., Dickinson, H., and, Twell, D., (2008) Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol. Plant, 1, 794-799.
40. Otegui, M., and, Staehelin, L.A., (2000) Cytokinesis in flowering plants: more than one way to divide a cell. Curr. Opin. Plant Biol. 3, 493-502.
41. Otegui, M.S., and, Staehelin, L.A., (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta, 218, 501-515. (Pubitemid 38285698)
42. Park, S.K., Howden, R., and, Twell, D., (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development, 125, 3789-3799. (Pubitemid 28488354)
43. Petersen, M., Brodersen, P., Naested, H., et al. (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103, 1111-1120. (Pubitemid 32037397)
44. Pitzschke, A., Djamei, A., Bitton, F., and, Hirt, H., (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant, 2, 120-137.
45. Qiu, J.L., Fiil, B.K., Petersen, K., et al. (2008a) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27, 2214-2221.
46. Qiu, J.L., Zhou, L., Yun, B.W., Nielsen, H.B., Fiil, B.K., Petersen, K., Mackinlay, J., Loake, G.J., Mundy, J., and, Morris, P.C., (2008b) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 148, 212-222. (Pubitemid 352847597)
47. Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.-C., Lee, P.Y., Truong, M.T., Beals, T.P., and, Goldberg, R.B., (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322. (Pubitemid 29087638)
48. Sasabe, M., Soyano, T., Takahashi, Y., Sonobe, S., Igarashi, H., Itoh, T.J., Hidaka, M., and, Machida, Y., (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, 1004-1014.
49. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and, Schneitz, K., (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 96, 11664-11669. (Pubitemid 29487438)
50. Scott, R.J., Spielman, M., and, Dickinson, H.G., (2004) Stamen structure and function. Plant Cell, 16 (Suppl), S46-S60. (Pubitemid 38774216)
51. Soyano, T., Nishihama, R., Morikiyo, K., Ishikawa, M., and, 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, 1055-1067. (Pubitemid 36459457)
52. Spielman, M., Preuss, D., Li, F.L., Browne, W.E., Scott, R.J., and, Dickinson, H.G., (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development, 124, 2645-2657. (Pubitemid 27341764)
53. Spurr, A.R., (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43.
54. Strompen, G., El Kasmi, F., Richter, S., Lukowitz, W., Assaad, F.F., Jurgens, G., and, Mayer, U., (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr. Biol. 12, 153-158. (Pubitemid 34102663)
55. Suarez-Rodriguez, M.C., Adams-Phillips, L., Liu, Y., Wang, H., Su, S.H., Jester, P.J., Zhang, S., Bent, A.F., and, Krysan, P.J., (2007) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143, 661-669. (Pubitemid 46940960)
56. Takahashi, Y., Soyano, T., Sasabe, M., and, Machida, Y., (2004) A MAP kinase cascade that controls plant cytokinesis. J. Biochem. 136, 127-132. (Pubitemid 39264965)
57. Takahashi, Y., Soyano, T., Kosetsu, K., Sasabe, M., and, 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.
58. Tanaka, H., Ishikawa, M., Kitamura, S., Takahashi, Y., Soyano, T., Machida, C., and, Machida, Y., (2004) The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells, 9, 1199-1211. (Pubitemid 39618534)
59. Twell, D., Park, S.K., Hawkins, T.J., Schubert, D., Schmidt, R., Smertenko, A., and, Hussey, P.J., (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat. Cell Biol. 4, 711-714. (Pubitemid 34993708)
60. Wang, S., Tiwari, S.B., Hagen, G., and, Guilfoyle, T.J., (2005) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell, 17, 1979-1993.
61. Wang, H., Liu, Y., Bruffett, K., Lee, J., Hause, G., Walker, J.C., and, Zhang, S., (2008a) 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. (Pubitemid 352843996)
62. Wang, S., Hubbard, L., Chang, Y., Guo, J., Schiefelbein, J., and, Chen, J.G., (2008b) Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biol. 8, 81.
63. Yang, W.C., Ye, D., Xu, J., and, Sundaresan, V., (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108-2117. (Pubitemid 29407351)
64. Yang, C.Y., Spielman, M., Coles, J.P., Li, Y., Ghelani, S., Bourdon, V., Brown, R.C., Lemmon, B.E., Scott, R.J., and, Dickinson, H.G., (2003a) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J. 34, 229-240. (Pubitemid 36540211)
65. Yang, S.L., Xie, L.F., Mao, H.Z., Puah, C.S., Yang, W.C., Jiang, L., Sundaresan, V., and, Ye, D., (2003b) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell, 15, 2792-2804. (Pubitemid 37546251)
66. Zhao, D., and, Ma, H., (2000) Male fertility: a case of enzyme identity. Curr. Biol. 10, R904-R907. (Pubitemid 32062649)
67. Zhao, D.Z., Wang, G.F., Speal, B., and, Ma, H., (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021-2031. (Pubitemid 34832928)
68. Zhou, C., Cai, Z., Guo, Y., and, Gan, S., (2009) An arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol. 150, 167-177.