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. 1999 Jan;11(1):101–113.

A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division.

L Bögre 1, O Calderini 1, P Binarova 1, M Mattauch 1, S Till 1, S Kiegerl 1, C Jonak 1, C Pollaschek 1, P Barker 1, N S Huskisson 1, H Hirt 1, E Heberle-Bors 1
PMCID: PMC144092  PMID: 9878635

Abstract

In eukaryotes, mitogen-activated protein kinases (MAPKs) are part of signaling modules that transmit diverse stimuli, such as mitogens, developmental cues, or various stresses. Here, we report a novel alfalfa MAPK, Medicago MAP kinase 3 (MMK3). Using an MMK3-specific antibody, we detected the MMK3 protein and its associated activity only in dividing cells. The MMK3 protein could be found during all stages of the cell cycle, but its protein kinase activity was transient in mitosis and correlated with the timing of phragmoplast formation. Depolymerization of microtubules by short treatments with the drug amiprophosmethyl during anaphase and telophase abolished MMK3 activity, indicating that intact microtubules are required for MMK3 activation. During anaphase, MMK3 was found to be concentrated in between the segregating chromosomes; later, it localized at the midplane of cell division in the phragmoplast. As the phragmoplast microtubules were redistributed from the center to the periphery during telophase, MMK3 still localized to the whole plane of division; thus, phragmoplast microtubules are not required to keep MMK3 at this location. Together, these data strongly support a role for MMK3 in the regulation of plant cytokinesis.

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Selected References

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  1. Asada T., Kuriyama R., Shibaoka H. TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci. 1997 Jan;110(Pt 2):179–189. doi: 10.1242/jcs.110.2.179. [DOI] [PubMed] [Google Scholar]
  2. Assaad F. F., Mayer U., Wanner G., Jürgens G. The KEULE gene is involved in cytokinesis in Arabidopsis. Mol Gen Genet. 1996 Dec 13;253(3):267–277. doi: 10.1007/pl00008594. [DOI] [PubMed] [Google Scholar]
  3. Banno H., Hirano K., Nakamura T., Irie K., Nomoto S., Matsumoto K., Machida Y. NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Mol Cell Biol. 1993 Aug;13(8):4745–4752. doi: 10.1128/mcb.13.8.4745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Binarova P., Cihalikova J., Dolezel J. Localization of MPM-2 recognized phosphoproteins and tubulin during cell cycle progression in synchronized Vicia faba root meristem cells. Cell Biol Int. 1993 Sep;17(9):847–856. doi: 10.1006/cbir.1993.1147. [DOI] [PubMed] [Google Scholar]
  5. Bogre L., Zwerger K., Meskiene I., Binarova P., Csizmadia V., Planck C., Wagner E., Hirt H., Heberle-Bors E. The cdc2Ms Kinase Is Differently Regulated in the Cytoplasm and in the Nucleus. Plant Physiol. 1997 Mar;113(3):841–852. doi: 10.1104/pp.113.3.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bowser J., Reddy A. S. Localization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J. 1997 Dec;12(6):1429–1437. doi: 10.1046/j.1365-313x.1997.12061429.x. [DOI] [PubMed] [Google Scholar]
  7. Calderini O., Bögre L., Vicente O., Binarova P., Heberle-Bors E., Wilson C. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. J Cell Sci. 1998 Oct;111(Pt 20):3091–3100. doi: 10.1242/jcs.111.20.3091. [DOI] [PubMed] [Google Scholar]
  8. Chan J., Rutten T., Lloyd C. Isolation of microtubule-associated proteins from carrot cytoskeletons: a 120 kDa map decorates all four microtubule arrays and the nucleus. Plant J. 1996 Aug;10(2):251–259. doi: 10.1046/j.1365-313x.1996.10020251.x. [DOI] [PubMed] [Google Scholar]
  9. Chiri S., De Nadai C., Ciapa B. Evidence for MAP kinase activation during mitotic division. J Cell Sci. 1998 Sep;111(Pt 17):2519–2527. doi: 10.1242/jcs.111.17.2519. [DOI] [PubMed] [Google Scholar]
  10. Earnest S., Khokhlatchev A., Albanesi J. P., Barylko B. Phosphorylation of dynamin by ERK2 inhibits the dynamin-microtubule interaction. FEBS Lett. 1996 Oct 28;396(1):62–66. doi: 10.1016/0014-5793(96)01074-5. [DOI] [PubMed] [Google Scholar]
  11. Glotzer M. The mechanism and control of cytokinesis. Curr Opin Cell Biol. 1997 Dec;9(6):815–823. doi: 10.1016/s0955-0674(97)80082-8. [DOI] [PubMed] [Google Scholar]
  12. Gotoh Y., Nishida E., Matsuda S., Shiina N., Kosako H., Shiokawa K., Akiyama T., Ohta K., Sakai H. In vitro effects on microtubule dynamics of purified Xenopus M phase-activated MAP kinase. Nature. 1991 Jan 17;349(6306):251–254. doi: 10.1038/349251a0. [DOI] [PubMed] [Google Scholar]
  13. Gu X., Verma D. P. Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division. Plant Cell. 1997 Feb;9(2):157–169. doi: 10.1105/tpc.9.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gu X., Verma D. P. Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J. 1996 Feb 15;15(4):695–704. [PMC free article] [PubMed] [Google Scholar]
  15. Heider H., Hug C., Lucocq J. M. A 40-kDa myelin basic protein kinase, distinct from erk1 and erk2, is activated in mitotic HeLa cells. Eur J Biochem. 1994 Jan 15;219(1-2):513–520. doi: 10.1111/j.1432-1033.1994.tb19966.x. [DOI] [PubMed] [Google Scholar]
  16. Hirt H., Mink M., Pfosser M., Bögre L., Györgyey J., Jonak C., Gartner A., Dudits D., Heberle-Bors E. Alfalfa cyclins: differential expression during the cell cycle and in plant organs. Plant Cell. 1992 Dec;4(12):1531–1538. doi: 10.1105/tpc.4.12.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hoshi M., Ohta K., Gotoh Y., Mori A., Murofushi H., Sakai H., Nishida E. Mitogen-activated-protein-kinase-catalyzed phosphorylation of microtubule-associated proteins, microtubule-associated protein 2 and microtubule-associated protein 4, induces an alteration in their function. Eur J Biochem. 1992 Jan 15;203(1-2):43–52. doi: 10.1111/j.1432-1033.1992.tb19825.x. [DOI] [PubMed] [Google Scholar]
  18. Jonak C., Kiegerl S., Ligterink W., Barker P. J., Huskisson N. S., Hirt H. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11274–11279. doi: 10.1073/pnas.93.20.11274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jonak C., Kiegerl S., Lloyd C., Chan J., Hirt H. MMK2, a novel alfalfa MAP kinase, specifically complements the yeast MPK1 function. Mol Gen Genet. 1995 Oct 25;248(6):686–694. doi: 10.1007/BF02191708. [DOI] [PubMed] [Google Scholar]
  20. Jonak C., Páy A., Bögre L., Hirt H., Heberle-Bors E. The plant homologue of MAP kinase is expressed in a cell cycle-dependent and organ-specific manner. Plant J. 1993 Apr;3(4):611–617. doi: 10.1046/j.1365-313x.1993.03040611.x. [DOI] [PubMed] [Google Scholar]
  21. Kovtun Y., Chiu W. L., Zeng W., Sheen J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature. 1998 Oct 15;395(6703):716–720. doi: 10.1038/27240. [DOI] [PubMed] [Google Scholar]
  22. Lauber M. H., Waizenegger I., Steinmann T., Schwarz H., Mayer U., Hwang I., Lukowitz W., Jürgens G. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol. 1997 Dec 15;139(6):1485–1493. doi: 10.1083/jcb.139.6.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lavoie J. N., L'Allemain G., Brunet A., Müller R., Pouysségur J. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem. 1996 Aug 23;271(34):20608–20616. doi: 10.1074/jbc.271.34.20608. [DOI] [PubMed] [Google Scholar]
  24. Liu B., Cyr R. J., Palevitz B. A. A kinesin-like protein, KatAp, in the cells of arabidopsis and other plants. Plant Cell. 1996 Jan;8(1):119–132. doi: 10.1105/tpc.8.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lukowitz W., Mayer U., Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 1996 Jan 12;84(1):61–71. doi: 10.1016/s0092-8674(00)80993-9. [DOI] [PubMed] [Google Scholar]
  26. Madhani H. D., Fink G. R. The riddle of MAP kinase signaling specificity. Trends Genet. 1998 Apr;14(4):151–155. doi: 10.1016/s0168-9525(98)01425-5. [DOI] [PubMed] [Google Scholar]
  27. Minshull J., Sun H., Tonks N. K., Murray A. W. A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell. 1994 Nov 4;79(3):475–486. doi: 10.1016/0092-8674(94)90256-9. [DOI] [PubMed] [Google Scholar]
  28. Mizoguchi T., Ichimura K., Shinozaki K. Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol. 1997 Jan;15(1):15–19. doi: 10.1016/S0167-7799(96)10074-3. [DOI] [PubMed] [Google Scholar]
  29. Morishima-Kawashima M., Kosik K. S. The pool of map kinase associated with microtubules is small but constitutively active. Mol Biol Cell. 1996 Jun;7(6):893–905. doi: 10.1091/mbc.7.6.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pay A., Heberle-Bors E., Hirt H. An alfalfa cDNA encodes a protein with homology to translationally controlled human tumor protein. Plant Mol Biol. 1992 Jun;19(3):501–503. doi: 10.1007/BF00023399. [DOI] [PubMed] [Google Scholar]
  31. Philipova R., Whitaker M. MAP kinase activity increases during mitosis in early sea urchin embryos. J Cell Sci. 1998 Sep;111(Pt 17):2497–2505. doi: 10.1242/jcs.111.17.2497. [DOI] [PubMed] [Google Scholar]
  32. Planchais S., Glab N., Tréhin C., Perennes C., Bureau J. M., Meijer L., Bergounioux C. Roscovitine, a novel cyclin-dependent kinase inhibitor, characterizes restriction point and G2/M transition in tobacco BY-2 cell suspension. Plant J. 1997 Jul;12(1):191–202. doi: 10.1046/j.1365-313x.1997.12010191.x. [DOI] [PubMed] [Google Scholar]
  33. Reszka A. A., Seger R., Diltz C. D., Krebs E. G., Fischer E. H. Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8881–8885. doi: 10.1073/pnas.92.19.8881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robinson M. J., Cobb M. H. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol. 1997 Apr;9(2):180–186. doi: 10.1016/s0955-0674(97)80061-0. [DOI] [PubMed] [Google Scholar]
  35. Sagata N. What does Mos do in oocytes and somatic cells? Bioessays. 1997 Jan;19(1):13–21. doi: 10.1002/bies.950190105. [DOI] [PubMed] [Google Scholar]
  36. Samuels A. L., Giddings T. H., Jr, Staehelin L. A. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol. 1995 Sep;130(6):1345–1357. doi: 10.1083/jcb.130.6.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shapiro P. S., Vaisberg E., Hunt A. J., Tolwinski N. S., Whalen A. M., McIntosh J. R., Ahn N. G. Activation of the MKK/ERK pathway during somatic cell mitosis: direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J Cell Biol. 1998 Sep 21;142(6):1533–1545. doi: 10.1083/jcb.142.6.1533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shiina N., Moriguchi T., Ohta K., Gotoh Y., Nishida E. Regulation of a major microtubule-associated protein by MPF and MAP kinase. EMBO J. 1992 Nov;11(11):3977–3984. doi: 10.1002/j.1460-2075.1992.tb05491.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sohrmann M., Schmidt S., Hagan I., Simanis V. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septum-inducing protein kinase Cdc7p. Genes Dev. 1998 Jan 1;12(1):84–94. doi: 10.1101/gad.12.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Staehelin L. A., Hepler P. K. Cytokinesis in higher plants. Cell. 1996 Mar 22;84(6):821–824. doi: 10.1016/s0092-8674(00)81060-0. [DOI] [PubMed] [Google Scholar]
  41. Takenaka K., Gotoh Y., Nishida E. MAP kinase is required for the spindle assembly checkpoint but is dispensable for the normal M phase entry and exit in Xenopus egg cell cycle extracts. J Cell Biol. 1997 Mar 10;136(5):1091–1097. doi: 10.1083/jcb.136.5.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Takenaka K., Moriguchi T., Nishida E. Activation of the protein kinase p38 in the spindle assembly checkpoint and mitotic arrest. Science. 1998 Apr 24;280(5363):599–602. doi: 10.1126/science.280.5363.599. [DOI] [PubMed] [Google Scholar]
  43. Tamemoto H., Kadowaki T., Tobe K., Ueki K., Izumi T., Chatani Y., Kohno M., Kasuga M., Yazaki Y., Akanuma Y. Biphasic activation of two mitogen-activated protein kinases during the cell cycle in mammalian cells. J Biol Chem. 1992 Oct 5;267(28):20293–20297. [PubMed] [Google Scholar]
  44. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Verlhac M. H., Kubiak J. Z., Clarke H. J., Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development. 1994 Apr;120(4):1017–1025. doi: 10.1242/dev.120.4.1017. [DOI] [PubMed] [Google Scholar]
  46. Wick S. M. Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol. 1991 Apr;3(2):253–260. doi: 10.1016/0955-0674(91)90149-s. [DOI] [PubMed] [Google Scholar]
  47. Wilson C., Anglmayer R., Vicente O., Heberle-Bors E. Molecular cloning, functional expression in Escherichia coli, and characterization of multiple mitogen-activated-protein kinases from tobacco. Eur J Biochem. 1995 Oct 1;233(1):249–257. doi: 10.1111/j.1432-1033.1995.249_1.x. [DOI] [PubMed] [Google Scholar]
  48. Wolniak S. M., Larsen P. M. The timing of protein kinase activation events in the cascade that regulates mitotic progression in Tradescantia stamen hair cells. Plant Cell. 1995 Apr;7(4):431–445. doi: 10.1105/tpc.7.4.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zecevic M., Catling A. D., Eblen S. T., Renzi L., Hittle J. C., Yen T. J., Gorbsky G. J., Weber M. J. Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J Cell Biol. 1998 Sep 21;142(6):1547–1558. doi: 10.1083/jcb.142.6.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]

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