Overexpression of a novel small peptide Rotundifolia4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana

Plant Journal

Volumn 38, Issue 4, 2004, Pages 699-713

  Narita, Noriyuki N ^a,b   Moore, Sally ^c,f   Horiguchi, Gorou ^a   Kubo, Minoru ^d   Demura, Taku ^d   Fukuda, Hiroo ^d,e   Goodrich, Justin ^c   Tsukaya, Hirokazu ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c Inst of Cell and Molecular Biology   (United Kingdom)

^d RIKEN Center for Sustainable Resource Science   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f Inst of Cell   (United Kingdom)

Author keywords

Arabidopsis thaliana; Cell proliferation; Leaf morphogenesis; ROT4; RTFL; Small peptide

Indexed keywords

CELLS; ENZYME KINETICS; FUSION REACTIONS; MUTAGENESIS; PLANT CELL CULTURE; PROTEINS;

CELL PROLIFERATION; TRANSGENIC PLANTS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; CYTOCHROME P450; MEMBRANE PROTEIN; PRIMER DNA; ROT4 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; CELL DIVISION; CHEMISTRY; CYTOLOGY; GENETICS; HISTOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CELL DIVISION; CYTOCHROME P-450 ENZYME SYSTEM; DNA PRIMERS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; SPERMATOPHYTA;

EID: 2542525473     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02078.x     Document Type: Article

References (68)

1. Adachi, J. and Hasegawa, M. (1996) MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likehood. Comput. Sci. Monogr. 28, 1-150.
2. An, Y.-Q., McDowell, J.M., Huang, S., McKinney, E.C., Chambliss, S. and Meagher, R.B. (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 10, 107-121.
3. Autran, D., Jonak, C., Belcram, K., Beemster, G.T., Kronenberger, J., Grandjean, O., Inzé, D. and Traas, J. (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J. 21, 6036-6049.
4. Byrne, M.E., Simorowski, J. and Martienssen, R.A. (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development, 129, 1957-1965.
5. Casson, S.A., Chilley, P.M., Toping, J.F., Evans, I.M., Souter, M.A. and Lindsey, K. (2002) The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell, 14, 1705-1721.
6. Cho, H.-T. and Cosgrove, D.J. (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 97, 9783-9788.
7. 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.
8. Cock, M.J. and McCormick, S. (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939-942.
9. Coen, E.S., Romero, J.M., Doyle, S., Elliott, R., Murphy, G. and Carpenter, R. (1990) FLORICAULA - a homeotic gene required for flower development in Antirrhinum majus. Cell, 63, 1311-1322.
10. De Veylder, L., Beeckman, T., Beemster, G.T., Krols, L., Terras, F., Landrieu, I., Van Der Schueren, E., Maes, S., Naudts, M. and Inzé, D. (2001) Functional analysis of cyclin-dependent linase inhibitors of Arabidopsis. Plant Cell, 13, 1653-4668.
11. De Veylder, L., Beeckman, T., Beemster, G.T. et al. (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J. 21, 1360-1368.
12. Dennison, K.L., Robertson, W.R., Lewis, B.D., Hirsch, R.E., Sussman, M.R. and Spalding, E.P. (2001) Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis. Plant Physiol. 127, 1012-1019.
13. Dewitte, W., Riou-Khamlichi, C., Scofield, S., Healy, J.M., Jacqmard, A., Kilby, N.J. and Murray, J.A. (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell, 15, 79-92.
14. Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E. and Dengler, N.G. (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419.
15. Drews, G.N., Bowman, J.L. and Meyerowitz, E.M. (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell, 65, 991-1002.
16. Elumalai, R.P., Nagpal, P. and Reed, J.W. (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell, 14, 119-131.
17. Eshed, Y., Baum, S.F., Perea, J.V. and Bowman, J.L. (2001) Establishment of polarity in lateral organs of plants. Curr. Biol. 11, 1251-1260.
18. Fletcher, J.C., Brand, U., Running, M.P., Simon, R. and Meyerowitz, E.M. (1999) Signaling of cell fate decisions by CLAVATA3 Arabidopsis shoot meristems. Science, 283, 1911-1914.
19. Frank, M.J. and Smith, L.G. (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr. Biol. 12, 849-853.
20. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M. and Coupland, G. (1997) A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature, 386, 44-51.
21. Hemerly, A., de Engler, J.A., Bergounioux, C., Van Montagu, M., Engler, G., Inzé, D. and Ferreira, P. (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14, 3925-3936.
22. Himi, S., Sano, R., Nishiyama, T., Tanahashi, T., Kato, M., Ueda, K. and Hasebe, M. (2001) Evolution of MADS-box gene induction by FLO/LFY genes. J. Mol. Evol. 53, 387-393.
23. Hobe, M., Muller, R., Grunewald, M., Brand, U. and Simon, R. (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213, 371-381.
24. Hu, Y., Bao, F. and Li, J. (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J. 24, 693-701.
25. Ito, T. and Meyerowitz, E.M. (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell, 12, 1541-1550.
26. Ito, T., Kim, G.-T. and Shinozaki, K. (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J. 22, 257-264.
27. Iwakawa, H., Ueno, Y., Semiarti, E. et al. (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 43, 467-478.
28. Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K. and Poethig, R.S. (2001) KANADI regulates organ polarity in Arabidopsis. Nature, 411, 706-709.
29. Kim, G.-T., Tsukaya, H. and Uchimiya, H. (1998a) The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana. Planta, 206, 175-183.
30. Kim, G.-T., Tsukaya, H. and Uchimiya, H. (1998b) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev. 12, 2381-2391.
31. Kim, G.-T., Tsukaya, H., Saito, Y. and Uchimiya, H. (1999) Changes in the shapes of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis. Proc. Natl. Acad. Sci. USA, 96, 9433-9437.
32. Kim, G.-T., Shoda, K., Tsuge, T., Cho, K.-H., Uchimiya, H., Yokoyama, R., Nihitani, K. and Tsukaya, H. (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J. 21, 1267-1279.
33. Krizek, B.A. (1999) Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev. Genet. 25, 224-236.
34. 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.
35. Matsubayashi, Y. and Sakagami, Y. (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. USA, 93, 7623-7627.
36. McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J. and Barton, M.K. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature, 411, 709-713.
37. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K. and Hirochika, H. (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell, 15, 1771-1780.
38. Mizukami, Y. and Fischer, R.L. (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc. Natl. Acad. Sci. USA, 97, 942-947.
39. Nakaya, M., Tsukaya, H., Murakami, N. and Kato, M. (2002) Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol. 43, 239-244.
40. Nath, U., Crawford, B.C., Carpenter, R. and Coen, E. (2003) Genetic control of surface curvature. Science, 299, 1404-1407.
41. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and Höfte, H. (1998) A plasma membrane-bound putative endo-1,4-β-D- glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17, 5563-5576.
42. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M. and Kobayashi, H. (1999) Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J. 18, 455-463.
43. Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C. and Weigel, D. (2003) Control of leaf morphogenesis by microRNAs. Nature, 425, 257-263.
44. Pearce, G., Strydom, D., Johnson, S. and Ryan, C.A. (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor protiens. Science, 253, 895-898.
45. Pearce, G., Moura, D.S., Stratmann, J. and Ryan, C.A., Jr (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl. Acad. Sci. USA, 98, 12843-12847.
46. Poethig, S. and Sussex, I.M. (1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta, 165, 170-184.
47. Ryan, C.A., Pearce, G., Scheer, J. and Moura, D.S. (2002) Polypeptide hormones. Plant Cell, 14 (Suppl.), S251-S264.
48. Sakakibara, K., Nishiyama, T., Kato, M. and Hasebe, M. (2001) Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Mol. Biol. Evol. 18, 491-502.
49. Sawa, S., Watanabe, K., Goto, K., Liu, Y.G., Shibata, D., Kanaya, E., Morita, E.H. and Okada, K. (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088.
50. Schopfer, C.R., Nasrallah, M.E. and Nasrallah, J.B. (1999) The male determinant of self-incompatibility in Brassica. Science, 286, 1697-1700.
51. Semiarti, E., Ueno, Y., Tsukaya, H., Iwakawa, H., Machida, C. and Machida, Y. (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression meristem-related homeobox genes in leaves. Development, 128, 1771-1783.
52. Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N. and Bowman, J.L. (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development, 126, 4117-4128.
53. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K. and McCann, M.C. (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 12, 1782-1786.
54. Sun, Y., Zhou, Q., Zhang, W., Fu, Y. and Huang, H. (2002) ASYMMETRIC LEAVES1, an Arabidopsis gene that is involved in the control of cell differentiation in leaves. Planta, 214, 694-702.
55. Takayama, S., Shiba, H., Iwano, M., Shimosato, H., Che, F.-S., Kai, N., Watanabe, M., Suzuki, G., Hinata, K. and Isogai, A. (2000) The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA, 97, 1920-1925.
56. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673-4680.
57. Tsuge, T., Tsukaya, H. and Uchimiya, H. (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development, 122, 1589-1600.
58. Tsukaya, H. (2002) Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int. Rev. Cytol. 217, 1-39.
59. Tsukaya, H. (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr. Opin. Plant Biol. 6, 57-62.
60. Tsukaya, H., Kozuka, T. and Kim, G.-T. (2002) Genetic control of petiole length in Arabidopsis thaliana. Plant Cell Physiol. 43, 1221-1228.
61. Ullah, H., Chen, J.-G., Young, J.C., Im, K.-H., Sussman, M.R. and Jones, A.M. (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science, 292, 2066-2069.
62. Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L. and Fowke, L.C. (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15, 501-510.
63. Wang, H., Zhou, Y., Gilmer, S., Whitwill, S. and Fowke, L.C. (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J. 24, 613-623.
64. Weigel, D., Ahn, J.H., Blazquez, M.A. et al. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003-1013.
65. Wen, J., Lease, K.A. and Walker, J.C. (2004) DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J. 37, 668-677.
66. Wilson, K., Long, D., Swinburne, J. and Coupland, G. (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell, 8, 659-671.
67. Yang, W.-C., Katinakis, P., Hendriks, P., Smolders, A., de Vries, F., Spee, J., van Kammen, A., Bisseling, T. and Franssen, H. (1993) Characterization of GmENOD40, a gene showing novel patterns of cell specific expression during soybean nodule development. Plant J. 3, 573-585.
68. Zhao, D., Yang, M., Solava, J. and Ma, H. (1999) The ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis. Dev. Genet. 25, 209-223.