Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense

Journal of Experimental Botany

Volumn 57, Issue 15, 2006, Pages 4171-4187

  Gray Mitsumune, Madoka ^a   O'Brien, Martin ^a   Bertrand, Charles ^b   Tebbji, Faiza ^a   Nantel, André ^c   Matton, Daniel P ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Carpel; Fruit development; MAPKKK; Ovule development; Solanaceae

Indexed keywords

GELS; GROWTH KINETICS; PLANTS (BOTANY); PROTEINS; RNA;

EXPRESSED SEQUENCE TAG (EST); HOMEOTIC GENE; PLANT FERTILIZATION; SOLANACEAE; SOLANUM CHACOENSE;

ENZYME KINETICS;

HOMEODOMAIN PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DNA MICROARRAY; ENZYMOLOGY; EXPRESSED SEQUENCE TAG; FERTILIZATION; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT SEED; PRENATAL DEVELOPMENT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SOLANUM;

AMINO ACID SEQUENCE; CELL DIFFERENTIATION; CLONING, MOLECULAR; EXPRESSED SEQUENCE TAGS; FERTILIZATION; FRUIT; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; MAP KINASE KINASE KINASES; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; PLANT PROTEINS; RNA, MESSENGER; SEEDS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION; SOLANUM;

MAGNOLIOPHYTA; SOLANACEAE; SOLANUM; SOLANUM CHACOENSE;

EID: 33845638024     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erl194     Document Type: Article

References (73)

1. Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, Dons HJ, van Tunen AJ. 1995. A novel class of MADS box genes is involved in ovule development in petunia. The Plant Cell 7, 1569-1582.
2. 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.
3. Becraft PW. 2002. Receptor kinase signaling in plant development. Annual Review of Cell and Developmental Biology 18, 163-192.
4. Becraft PW, Asuncion-Crabb Y. 2000. Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127, 4039-4048.
5. Bergmann DC, Lukowitz W, Somerville CR. 2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304, 1494-1497.
6. Busi MV, Bustamante C, D'Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E. 2003. MADS-box genes expressed during tomato seed and fruit development. Plant Molecular Biology 52, 801-815.
7. Bussière F, Ledû S, Girard M, Héroux M, Perreault J-P, Matton DP. 2003. Development of an efficient cis-trans-cis ribozyme cassette to inactivate plant genes. Plant Biotechnology Journal 1, 423-435.
8. Canales C, Bhatt AM, Scott R, Dickinson H. 2002. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Current Biology 12, 1718-1727.
9. Chevalier D, Batoux M, Fulton L, Pfister K, Yadav RK, Schellenberg M, Schneitz K. 2005. STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proceedings of the National Academy of Sciences, USA 102, 9074-9079.
10. Clark SE, Running MP, Meyerowitz EM. 1993. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119, 397-418.
11. Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ. 1995. The petunia MADS box gene FBP11 determines ovule identity. The Plant Cell 7, 1859-1868.
12. Colombo L, Franken J, Van der Krol AR, Wittich PE, Dons HJ, Angenent GC. 1997. Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. The Plant Cell 9, 703-715.
13. Conner J, Liu Z. 2000. LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proceedings of the National Academy of Sciences, USA 97, 12902-12907.
14. Drews GN, Bowman JL, Meyerowitz EM. 1991. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991-1002.
15. Elion EA. 2000. Pheromone response, mating and cell biology. Current Opinion in Microbiology 3, 573-581.
16. Fanger GR, Gerwins P, Widmann C, Jarpe MB, Johnson GL. 1997. MEKKs, GCKs, MLKs, PAKs, TAKs, and tpls: upstream regulators of the c-Jun amino-terminal kinases? Current Opinion in Genetics and Development 7, 67-74.
17. Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L. 2003. MADS-box protein complexes control carpel and ovule development in Arabidopsis. The Plant Cell 15, 2603-2611.
18. Gasser CS, Broadhvest J, Hauser BA. 1998. Genetic analysis of ovule development. Annual Review in Plant Physiology and Plant Molecular Biology 49, 1-24.
19. Germain H, Rudd S, Zotti C, Caron S, O'Brien M, Chantha S-C, Lagacé M, Major F, Matton DP. 2005. A 6374 unigene set corresponding to low abundance transcripts expressed following fertilization in Solanum chacoense Bitt., and characterization of 30 receptor-like kinases. Plant Molecular Biology 59, 513-529.
20. Gifford ML, Dean S, Ingram GC. 2003. The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130, 4249-4258.
21. Hanks SK, Hunter T. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB Journal 9, 576-596.
22. Hanks SK, Quinn AM. 1991. Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods in Enzymology 200, 38-62.
23. Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC. 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology 127, 803-816.
24. Hirt H. 2000. MAP kinases in plant signal transduction. Results of Problems in Cell Differentiation 27, 1-9.
25. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254-267.
26. Ito T, Takahashi N, Shimura Y, Okada K. 1997. A serine/threonine protein kinase gene isolated by an in vivo binding procedure using the Arabidopsis floral homeotic gene product, AGAMOUS. Plant and Cell Physiology 38, 248-258.
27. Jack T. 2001. Plant development going MADS. Plant Molecular Biology 46, 515-520.
28. Jones JDG, Dunsmuir P, Bedbrook J. 1985. High level expression of introduced chimeric genes in regenerated transformed plants. The EMBO Journal 4, 2411-2418.
29. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427-441.
30. Kramer EM, Jaramillo MA, Di Stilio VS. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166, 1011-1023.
31. Lee H-S, Chung Y-Y, Das C, Karunanandaa B, van Went JL, Mariani C, Kao T-H. 1997. Embryo sac development is affected in Petunia inflata plants transformed with an antisense gene encoding the extracellular domain of receptor kinase PRK1. Sexual Plant Reproduction 10, 341-350.
32. Lee H-S, Karunanandaa B, McCubbin A, Gilroy S, Kao T-h. 1996. PRK1, a receptor-like kinase of Petunia inflata, is essential for postmeiotic development of pollen. The Plant Journal 9, 613-624.
33. Li J, Chory J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.
34. Liu Z, Franks RG, Klink VP. 2000. Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. The Plant Cell 12, 1879-1892.
35. Liu Z, Meyerowitz EM. 1995. LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975-991.
36. Lorbiecke R, Steffens M, Tomm JM, Scholten S, von Wiegen P, Kranz E, Wienand U, Sauter M. 2005. Phytosulphokine gene regulation during maize (Zea mays L.) reproduction. Journal of Experimental Botany 56, 1805-1819.
37. Lukowitz W, Roeder A, Parmenter D, Somerville C. 2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116, 109-119.
38. Madhani HD, Fink GR. 1998. The riddle of MAP kinase signaling specificity. Trends in Genetics 14, 151-155.
39. Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF. 1992. Manipulation of flower structure in transgenic tobacco. Cell 71, 133-143.
40. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. 2002. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296, 1470-1472.
41. Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M. 1997. Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. The Plant Cell 9, 1757-1766.
42. Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW. 1994. Homeotic transformation of ovules into carpel-like structures in Arabidopsis. The Plant Cell 6, 333-349.
43. Murphy LO, Blenis J. 2006. MAPK signal specificity: the right place at the right time. Trends in Biochemical Science 31, 268-275.
44. Nadeau JA, Sack FD. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296, 1697-1700.
45. Nishihama R, Banno H, Shibata W, Hirano K, Nakashima M, Usami S, Machida Y. 1995. Plant homologues of components of MAPK (mitogen-activated protein kinase) signal pathways in yeast and animal cells. Plant and Cell Physiology 36, 749-757.
46. O'Brien M, Bertrand C, Matton DP. 2002a. Characterization of a fertilization-induced and developmentally regulated plasma-membrane aquaporin expressed in reproductive tissues, in the wild potato Solanum chacoense Bitt. Planta 215, 485-493.
47. O'Brien M, Chantha SC, Rahier A, Matton DP. 2005. Lipid signaling in plants. cloning and expression analysis of the obtusifoliol 14a-demethylase from Solanum chacoense Bitt., a pollination- and fertilization-induced gene with both obtusifoliol and lanosterol demethylase activity. Plant Physiology 139, 734-749.
48. O'Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP. 2002b. Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. The Plant Journal 32, 985-996.
49. O'Brien M, Gray-Mitsumune M, Kapfer C, Bertrand C, Matton DP. 2006. The ScFRK2 MAP kinase kinase kinase from Solanum chacoense affects pollen development and viability. Planta (in press).
50. Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424, 85-88.
51. Piwien-Pilipuk G, Huo JS, Schwartz J. 2002. Growth hormone signal transduction. Journal of Pediatric Endocrinology and Metabolism 15, 771-786.
52. Posas F, Saito H. 1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276, 1702-1705.
53. Ray A, Robinson-Beers K, Ray S, Baker SC, Lang JD, Preuss D, Milligan SB, Gasser CS. 1994. Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proceedings of the National Academy of Sciences, USA 91, 5761-5765.
54. Robinson MJ, Cobb MH. 1997. Mitogen-activated protein kinase pathways. Current Opinion in Cell Biology 9, 180-186.
55. Romeis T. 2001. Protein kinases in the plant defence response. Current Opinion in Plant Biology 4, 407-414.
56. Saitou N, Nei M. 1987. The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
57. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
58. Samuel MA, Ellis BE. 2002. Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. The Plant Cell 14, 2059-2069.
59. Schmidt ED, Guzzo F, Toonen MA, de Vries SC. 1997. A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124, 2049-2062.
60. Schneitz K, Hulskamp M, Kopczak SD, Pruitt RE. 1997. Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 124, 1367-1376.
61. Sells MA, Knaus UG, Bagrodia S, Ambrose DM, Bokoch GM, Chernoff J. 1997. Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Current Biology 7, 202-210.
62. Sugden PH, Clerk A. 1997. Regulation of the ERK subgroup of MAP kinase cascades through G protein-coupled receptors. Cell Signaling 9, 337-351.
63. Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y. 2002. ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant and Cell Physiology 43, 419-428.
64. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882.
65. Tieman DM, Ciardi JA, Taylor MG, Klee HJ. 2001. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. The Plant Journal 26, 47-58.
66. Tonaco IA, Borst JW, de Vries SC, Angenent GC, Immink RG. 2006. In vivo imaging of MADS-box transcription factor interactions. Journal of Experimental Botany 57, 33-42.
67. Treisman R. 1996. Regulation of transcription by MAP kinase cascades. Current Opinion in Cell Biology 8, 205-215.
68. Tu H, Barr M, Dong DL, Wigler M. 1997. Multiple regulatory domains on the Byr2 protein kinase. Molecular and Cellular Biology 17, 5876-5887.
69. Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T. 2003. Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. The Plant Cell 15, 2680-2693.
70. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution 18, 691-699.
71. Wilkinson J, Twell D, Lindsey K. 1997. Activities of CaMV 35S and nos promoters in pollen: implications for field release of transgenic plants. Journal of Experimental Botany 48, 265-275.
72. Wu C, Leberer E, Thomas DY, Whiteway M. 1999. Functional characterization of the interaction of Ste50p with Ste11p MAPKKK in Saccharomyces cerevisiae. Molecular Biology of the Cell 10, 2425-2440.
73. Zhang S, Klessig DF. 2001. MAPK cascades in plant defense signaling. Trends in Plant Science 6, 520-527.