Perturbation of cytokinin and ethylene-signalling pathways explain the strong rooting phenotype exhibited by Arabidopsis expressing the Schizosaccharomyces pombe mitotic inducer, cdc25

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Spadafora, Natasha D ^a,b   Parfitt, David ^a   Marchbank, Angela ^a   Li, Sherong ^a   Bruno, Leonardo ^b   Vaughan, Rhys ^a   Nieuwland, Jeroen ^a   Buchanan Wollaston, Vicky ^c   Herbert, Robert J ^d   Bitonti, Maria B ^b   Doonan, John ^e   Albani, Diego ^f   Prinsen, Els ^g   Francis, Dennis ^a   Rogers, Hilary J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALABRIA   (Italy)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF WORCESTER   (United Kingdom)

^e ABERYSTWYTH UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF SASSARI   (Italy)

^g UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA; NICOTIANA TABACUM; SCHIZOSACCHAROMYCES POMBE; TRACHEOPHYTA;

CDC25 PROTEIN, S POMBE; CYTOKININ; ETHYLENE; ETHYLENE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARABIDOPSIS; ARTICLE; DARKNESS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; PHENOTYPE; PLANT GENE; PLANT GROWTH; PLANT ROOT; SCHIZOSACCHAROMYCES; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; CYTOKININS; DARKNESS; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYPOCOTYL; INDOLEACETIC ACIDS; MITOSIS; PHENOTYPE; PHOSPHOPROTEIN PHOSPHATASES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84862792000     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-45     Document Type: Article

References (55)

1. Sorrell DA, Menges M, Healy JMS, Deveaux Y, Amano C, Su Y, Nakagami H, Shinmyo A, Doonan J, Sekine M, Murray JAH. Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar Bright Yellow-2 cells. Plant Physiol 2001, 126:1214-1223. 10.1104/pp.126.3.1214, 116477, 11457971.
2. Featherstone C, Russell P. Fission yeast p107wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 1991, 349:808-811. 10.1038/349808a0, 1825699.
3. Russell P, Nurse P. cdc25+ functions as an inducer of mitotic control of fission yeast. Cell 1986, 45:145-153. 10.1016/0092-8674(86)90546-5, 3955656.
4. Sun Y, Dilkes BP, Zhang C, Dante RA, Carneiro NP, Lowe KS, Jug R, Gordon-Kamm WJ, Larkins BA. Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc Natl Acad Sci USA 1999, 96:4180-4185. 10.1073/pnas.96.7.4180, 22441, 10097184.
5. Sorrell DA, Marchbank A, McMahon K, Dickinson JR, Rogers HJ, Francis D. A WEE1 homologue from Arabidopsis thaliana. Planta 2002, 215:518-522. 10.1007/s00425-002-0815-4, 12111237.
6. Gonzalez N, Hernould M, Delmas F, Gevaudant F, Duffe P, Causse M, Mouras A, Chevalier C. Molecular characterization of a WEE1 gene homologue in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol 2004, 56:849-861. 10.1007/s11103-004-5110-2, 15821985.
7. Khadaroo B, Robbens S, Ferraz C, Derelle E, Eychenie S, Cooke R, Peaucellier G, Delseny M, Demaille J, Van de Peer Y, et al. The first green lineage cdc25 dual-specificity phosphatase. Cell Cycle 2004, 3:513-518.
8. Landrieu I, da Costa M, De Veylder L, Dewitte F, Vandepoele K, Hassan S, Wieruszeski J-M, Faure J-D, Van Montague M, Inze D, Lippens G. A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc Nat Acad Sc USA 2004, 101:13380-13385.
9. Sorrell DA, Chrimes D, Dickinson JR, Rogers HJ, Francis D. The Arabidopsis CDC25 induces a short cell length when over expressed in fission yeast: evidence for cell cycle function. New Phytol 2005, 165:425-428.
10. Spadafora ND, Doonan JH, Herbert RJ, Bitonti NB, Wallace E, Rogers HJ, Francis D. Arabidopsis T-DNA insertional lines for CDC25 are hypersensitive to hydroxyurea but not to zeocin or salt stress. Ann Bot 2011, 107:1183-1192. 10.1093/aob/mcq142, 20647223.
11. Bleeker PM, Hakvoort HWJ, Bliek M, Souer E, Schat H. Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 2006, 45:917-929. 10.1111/j.1365-313X.2005.02651.x, 16507083.
12. Dhankher OP, Rosen BP, McKinney EC, Meagher RB. Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase(ACR 2). Proc Nat Acad Sci 2006, 103:5413-5418. 10.1073/pnas.0509770102, 1459369, 16567632.
13. Zhang K, Letham DS, John PC. Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase. Planta 1996, 200:2-12.
14. Zhang K, Diderich L, John PCL. The cytokinin requirement for cell division in cultured Nicotiana plumbaginofolia cells can be satisfied by yeast Cdc25 tyrosine phosphatase. Implications for mechanisms of cytokinin response and plant development. Plant Physiol 2005, 137:308-316. 10.1104/pp.104.051938, 548861, 15618425.
15. Bell MH, Halford NG, Ormrod JC, Francis D. Tobacco plants transformed with cdc25, a mitotic inducer gene from fission yeast. Plant Mol Biol 1993, 23:445-451. 10.1007/BF00019293, 8219080.
16. McKibbin R, Halford NG, Francis D. Expression of fission yeast cdc25 alters the frequency of lateral root formation in transgenic tobacco. Plant Mol Biol 1998, 36:601-612. 10.1023/A:1005937011095, 9484455.
17. Orchard CB, Siciliano I, Sorrell D, Marchbank A, Rogers HJ, Francis D, Herbert RJ, Suchomelova P, Lipavska H, Azmi A, Van Onckelen H. Tobacco BY-2 cells expressing fission yeast cdc25 bypass a G2/M block on the cell cycle. Plant J 2005, 44:290-299. 10.1111/j.1365-313X.2005.02524.x, 16212607.
18. Redig P, Shaul O, Inze D, Van Montagu M, Van Onckelen H. Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY-2 cells. FEBS Lett 1996, 391:175-180. 10.1016/0014-5793(96)00728-4, 8706911.
19. Laureys F, Dewitte W, Witters E, Van Montagu M, Inze D, Van Onckelen H. Zeatin is indispensable for the G2-M transition in tobacco BY-2 cells. FEBS Lett 1998, 426:29-32. 10.1016/S0014-5793(98)00297-X, 9598972.
20. Suchomelova P, Velgova D, Masek T, Francis D, Rogers HJ, Marchbank AM, Lipavska H. The fission yeast cell cycle regulator, cdc25, induces de novo shoot formation in tobacco: evidence of a cytokinin-like effect. Plant Physiol Biochem 2004, 42:49-55. 10.1016/j.plaphy.2003.10.010, 15061084.
21. Teichmanová M, Mašková P, Vojvodová P, Krekule J, Francis D, Lipavská H. The fission yeast mitotic activator, cdc25, and sucrose induce early flowering synergistically in the day-neutral Nicotiana tabacum cv. Samsun. New Phytol 2007, 176:804-812.
22. Sorrell DA, Marchbank AM, Chrimes DA, Dickinson JR, Rogers HJ, Francis D, Grierson CS, Halford NG. The Arabidopsis 14-3-3 protein, GF14ω, binds to the Schizosaccharomyces pombe Cdc25 phosphatase and rescues checkpoint defects in the rad24- mutant. Planta 2003, 218:50-57. 10.1007/s00425-003-1083-7, 12942327.
23. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 2001, 409:1060-1063. 10.1038/35059117, 11234017.
24. Guo H, Ecker JR. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 2003, 115:667. 10.1016/S0092-8674(03)00969-3, 14675532.
25. Eisinger W. Regulation of pea internode expansion by ethylene. Ann Rev Plant Physiol 1983, 34:225-240.
26. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmu{double acute}lling T. Cytokinin-deficient transgenic Arabidopsis plant show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 2003, 15:2532-2550. 10.1105/tpc.014928, 280559, 14555694.
27. Riefler M, Novak O, Strnad M, Schmülling T. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed Size, germination, root development, and cytokinin metabolism. Plant Cell 2006, 18:40-54. 10.1105/tpc.105.037796, 1323483, 16361392.
28. Mok DW, Mok MC. Cytokinin metabolism and action. Ann Rev Plant Physiol Plant Mol Biol 2001, 52:89-118.
29. Hirose N, Makita N, Yamaya T, Sakakibara H. Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol 2005, 138:196-206. 10.1104/pp.105.060137, 1104175, 15849298.
30. Kudo T, Kiba T, Sakibara H. Metabolism and long-distance translocation of cytokinins. J Integ Plant Biol 2010, 52:53-60.
31. Sun J, Hirose N, Wang X, Wen P, Xue L, Sakakibara H, Zuo J. Arabidopsis SOI33/AtENT8 gene encodes a putative equilibrative nucleoside transporter that is involved in cytokinin transport in planta. J Integ Plant Biol 2005, 47:588-603.
32. Kakimoto T. Perception and signal transduction of cytokinins. Ann Rev Plant Biol 2003, 54:605-627.
33. Malamy JE, Benfey PN. Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci 1997, 2:390-396.
34. Rost TL. The organization of roots of dicotyledonous plants and the positions of control points. Ann Bot 2011, 107:1213-1222. 10.1093/aob/mcq229, 21118839.
35. Veselý J, Havliček L, Strnad M, Blow JJ, Donella-deana A, Pinna L, Letham DS, Kato J, Detivaud L, Leclerc S, Meijer L. Inhibition of cyclin-dependent kinases by purine analogues. Eur J Biochem 1994, 224:771-786. 10.1111/j.1432-1033.1994.00771.x, 7925396.
36. Celenza JL, Grisafi PL, Fink GR. A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 1995, 9:2131-2142. 10.1101/gad.9.17.2131, 7657165.
37. Fukaki H, Okushima Y, Tasaka M. Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 2007, 256:111-137.
38. Schüepp O. Untersuchen über Wachstum und Formwechsel von Vetationspunkten. Jahrbuch Wiss Botanik 1917, 57:17-79.
39. Lipavská H, Mašková P, Vojvodová P. Regulatory dephoshorylation of CDK at G2/M in plants: yeast mitotic phosphatase cdc25 induces cytokinin-like effects in transgenic tobacco morphogenesis. Ann Bot 2011, 107:1071-1086. 10.1093/aob/mcr016, 21339187.
40. Ortega-Martinez O, Pernas M, Carol RJ, Dolan L. Ethylene modulates stem-cell division in the Arabidopsis thaliana root. Science 2007, 317:507-510. 10.1126/science.1143409, 17656722.
41. Neljubow D. Uber die horizontale Nutation der Stengel von Pisum sativum und einiger anderen Pflanzen. Beihrage und Botanik Zentralblatt 1901, 10:128-139.
42. Barlow PW. The effect of ethylene on root meristems of Pisum sativum and Zea mays. Planta 1976, 131:235-243.
43. Ponce G, Barlow PW, Feldman LJ, Cassab GI. Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size and pattern of cap cell differentiation in maize. Plant Cell Env 2005, 28:719-732.
44. Clough SJ, Bent AJ. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998, 16:735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.
45. Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 1962, 15:473-479.
46. Armstrong SW, Francis D. Differences in cell cycle duration of sister cells in secondary root meristems of Cocos nucifera L. Ann Bot 1985, 56:803-814.
47. Perilli S, Sabatini S. Analysis of root meristem size development. Plant Developmental Biology, Methods in Molecular Biology 2010, 177-187. Heidelberg: Springer, Henig L, Köhler C.
48. Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J. A map of KNAT gene expression in the Arabidopsis root. Plant Mol Biol 2006, 60:1-20. 10.1007/s11103-005-1673-9, 16463096.
49. Parfitt D, Herbert RJ, Rogers HJ, Francis D. Differential expression of putative floral genes in Pharbitis nil shoot apices cultured on glucose compared with sucrose. J Exp Bot 2004, 55:2169-2177. 10.1093/jxb/erh234, 15361540.
50. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2_DDCT method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
51. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 2004, 38:366-379. 10.1111/j.1365-313X.2004.02051.x, 15078338.
52. Allemeersch J, Durinck S, Vanderhaeghen R, Alard P, Maes R, Seeuws K, Bogaert T, Coddens K, Deschouwer K, Van Hummelen P, Vuylsteke M, Moreau Y, Kwekkeboom J, Wijfjes AHM, May S, Beynon J, Hilson P, Kuiper MTR. Benchmarking the CATMA microarray: a novel tool for Arabidopsis transcriptome analysis. Plant Physiol 2005, 137:588-601. 10.1104/pp.104.051300, 1065359, 15710687.
53. Bieleski RL. The problem of halting enzyme action when extracting plant tissues. Anal Biochem 1964, 121:431-442.
54. Prinsen E, Van Dongen W, Esmans EL, Van Onckelen H. Micro and Capillary LC-MS/MS: A New Dimension in Phytohormone Research. J Chromatog 1998, 826:25-37.
55. Prinsen E, Van-Laer S, Oden S, Van-Onckelen H. Auxin analysis. Plant hormone protocols 2000, 49-65. Totowa: Humana Press, Tucker GA.