Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development

Plant Cell

Volumn 20, Issue 3, 2008, Pages 602-613

  Wang, Huachun ^a   Liu, Yidong ^a   Bruffett, Kristin ^a   Lee, Justin ^b   Hause, Gerd ^c   Walker, John C ^d   Zhang, Shuqun ^a  

^a University of Missouri   (United States)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

ARABIDOPSIS PROTEIN; ATMPK3 PROTEIN, ARABIDOPSIS; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MPK6 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PLANT INFERTILITY; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICROSCOPY, ELECTRON, SCANNING; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; PLANT INFERTILITY; PLANTS, GENETICALLY MODIFIED;

EID: 48249150428     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.058032     Document Type: Article

References (59)

1. Acosta-Garcia, G., and Vielle-Calzada, J.-P. (2004). A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16: 2614-2628.
2. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M., and Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
3. Bajon, C., Horlow, C., Motamayor, J.C., Sauvanet, A., and Robert, D. (1999). Megasporogenesis in Arabidopsis thaliana L.: An ultrastructural study. Sex. Plant Reprod. 12: 99-109.
4. Balasubramanian, S., and Schneitz, K. (2000). NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana. Development 127: 4227-4238.
5. Bergmann, D.C., Lukowitz, W., and Somerville, C.R. (2004). Stomatal development and pattern controlled by a MAPKK kinase. Science 304: 1494-1497.
6. Broadhvest, J., Baker, S.C., and Gasser, C.S. (2000). SHORT INTEGUMENTS 2 promotes growth during Arabidopsis reproductive development. Genetics 155: 899-907.
7. Bush, S.M., and Krysan, P.J. (2007). Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J. Exp. Bot. 58: 2181-2191.
8. Chang, L., and Karin, M. (2001). Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
9. Chou, S., Huang, L., and Liu, H. (2004). Fus3-regulated Tec1 degradation through SCFCdc4 determines MAPK signaling specificity during mating in yeast. Cell 119: 981-990.
10. Christensen, C.A., Gorsich, S.W., Brown, R.H., Jones, L.G., Brown, J., Shaw, J.M., and Drews, G.N. (2002). Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 14: 2215-2232.
11. Christensen, C.A., King, E.J., Jordan, J.R., and Drews, G.N. (1997). Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10: 49-64.
12. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
13. Dard, N., and Peter, M. (2006). Scaffold proteins in MAP kinase signaling: More than simple passive activating platforms. Bioessays 28: 146-156.
14. Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q.J., Gerentes, D., Perez, P., and Smyth, D.R. (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8: 155-168.
15. Franks, R.G., Wang, C., Levin, J.Z., and Liu, Z. (2002). SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129: 253-263.
16. Golden, T.A., Schauer, S.E., Lang, J.D., Pien, S., Mushegian, A.R., Grossniklaus, U., Meinke, D.W., and Ray, A. (2002). SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol. 130: 808-822.
17. Guilford, V.B., and Fisk, E.L. (1951). Megasporogenesis and seed development in Mimulus tigrinus and Torenia fournieri. Bull. Torrey Bot. Club 79: 6-24.
18. Hamel, L.P., et al. (2006). Ancient signals: Comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 11: 192-198.
19. Higashiyama, T., Kuroiwa, H., Kawano, S., and Kuroiwa, T. (1997). Kinetics of double fertilization in Torenia fournieri based on direct observations of the naked embryo sac. Planta 203: 101-110.
20. Huang, B.Q., and Russell, S.D. (1992). Female germ unit - Organization, isolation, and function. Int. Rev. Cytol. 140: 233-293.
21. Ichimura, K., Shinozaki, K., Tena, G., Sheen, J., Henry, Y., Champion, A., Kreis, M., Zhang, S., and Hirt, H. (2002). Mitogen-activated protein kinase cascades in plants: A new nomenclature. Trends Plant Sci. 7: 301-308.
22. Klucher, K.M., Chow, H., Reiser, L., and Fischer, R.L. (1996). The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8: 137-153.
23. Kolch, W. (2005). Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6: 827-837.
24. Lecuit, T., and Lenne, P.F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8: 633-644.
25. Liu, C.M., and Meinke, D.W. (1998). The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J. 16: 21-31.
26. Liu, Y., and 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.
27. Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
28. Meister, R.J., Kotow, L.M., and Gasser, C.S. (2002). SUPERMAN attenuates positive INNER NO OUTER autoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 129: 4281-4289.
29. Miles, G.P., Samuel, M.A., Zhang, Y., and Ellis, B.E. (2005). RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. Environ. Pollut. 138: 230-237.
30. Misra, R.C. (1962). Contribution to the embryology of Arabidopsis thaliana (GAY & MONN.). Agra. Univ. J. Res. Sci. 11: 191-199.
31. Mor, A., and Philips, M.R. (2006). Compartmentalized Ras/MAPK signaling. Annu. Rev. Immunol. 24: 771-800.
32. Morrison, D.K., and Davis, R.J. (2003). Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu. Rev. Cell Dev. Biol. 19: 91-118.
33. Nakagami, H., Pitzschke, A., and Hirt, H. (2005). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10: 339-346.
34. Pedley, K.F., and Martin, G.B. (2005). Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol. 8: 541-547.
35. Pillitteri, L.J., Bemis, S.M., Shpak, E.D., and Torii, K.U. (2007). Haploinsufficiency after successive loss of signaling reveals a role for ERECTA-family genes in Arabidopsis ovule development. Development 134: 3099-3109.
36. Ray, A., Robinson-Beers, K., Ray, S., Baker, S.C., Lang, J.D., Preuss, D., Milligan, S.B., and Gasser, C.S. (1994). Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc. Natl. Acad. Sci. USA 91: 5761-5765.
37. Reiser, L., Modrusan, Z., Margossian, L., Samach, A., Ohad, N., Haughn, G.W., and Fischer, R.L. (1995). The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83: 735-742.
38. Remenyi, A., Good, M.C., Bhattacharyya, R.P., and Lim, W.A. (2005). The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol. Cell 20: 951-962.
39. Ren, D., Yang, H., and Zhang, S. (2002). Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277: 559-565.
40. Robinson-Beers, K., Pruitt, R.E., and Gasser, C.S. (1992). Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4: 1237-1249.
41. Rodkiewicz, B. (1970). Callose in cell walls during megasporogenesis in angiosperms. Planta 93: 39-47.
42. Roe, J.L., Nemhauser, J.L., and Zambryski, P.C. (1997). TOUSLED participates in apical tissue formation during gynoecium development in Arabidopsis. Plant Cell 9: 335-353.
43. Schneitz, K., Hulskamp, M., and Pruitt, R.E. (1995). Wild-type ovule development in Arabidopsis thaliana: A light microscope study of cleared whole-mount tissue. Plant J. 7: 731-749.
44. Schwartz, M.A., and Madhani, H.D. (2004). Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu. Rev. Genet. 38: 725-748.
45. Shpak, E.D., Berthiaume, C.T., Hill, E.J., and Torii, K.U. (2004). Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131: 1491-1501.
46. Tena, G., Asai, T., Chiu, W.L., and Sheen, J. (2001). Plant mitogen-activated protein kinase signaling cascades. Curr. Opin. Plant Biol. 4: 392-400.
47. Vaudry, D., Stork, P.J., Lazarovici, P., and Eiden, L.E. (2002). Signaling pathways for PC12 cell differentiation: Making the right connections. Science 296: 1648-1649.
48. Vielle-Calzada, J.P., Baskar, R., and Grossniklaus, U. (2000). Delayed activation of the paternal genome during seed development. Nature 404: 91-94.
49. Villanueva, J.M., Broadhvest, J., Hauser, B.A., Meister, R.J., Schneitz, K., and Gasser, C.S. (1999). INNER NO OUTER regulates abaxial- adaxial patterning in Arabidopsis ovules. Genes Dev. 13: 3160-3169.
50. Wallwork, M.A.B., and Sedgley, M. (2000). Early events in the penetration of the embryo sac in Torenia fournieri (Lind.). Ann. Bot. (Lond.) 85: 447-454.
51. Wang, H., Chevalier, D., Larue, C., Ki Cho, S., and Walker, J.C. (2007b). The protein phosphatases and protein kinases of Arabidopsis thaliana. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0106, http://www.aspb.org/publications/arabidopsis/.
52. Wang, H., Ngwenyama, N., Liu, Y., Walker, J.C., and Zhang, S. (2007a). Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63-73.
53. Widmann, C., Gibson, S., Jarpe, M.B., and Johnson, G.L. (1999). Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79: 143-180.
54. Yadegari, R., and Drews, G.N. (2004). Female gametophyte development. Plant Cell 16: S133-S142.
55. Yang, K.-Y., Liu, Y., and Zhang, S. (2001). Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98: 741-746.
56. Yang, W.-C., and Sundaresan, V. (2000). Genetics of gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. 3: 53-57.
57. Zhang, S., and Klessig, D.F. (1997). Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9: 809-824.
58. Zhang, S., and Klessig, D.F. (1998). The tobacco wounding-activated MAP kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA 95: 7225-7230.
59. Zhang, S., and Klessig, D.F. (2001). MAPK cascades in plant defense signaling. Trends Plant Sci. 6: 520-527.