Organ size regulation in plants: Insights from compensation

Frontiers in Plant Science

Volumn 2, Issue JUL, 2011, Pages

  Horiguchi, Gorou ^a   Tsukaya, Hirokazu ^b  

^a RIKKYO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Angustifolia3; Cell expansion; Cell proliferation; Compensation; Extra small sisters; Fugu; Oligocellula; Organ size

Indexed keywords

EID: 84856580517     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2011.00024     Document Type: Article

References (65)

1. Anastasiou, E., Kenz, S., Gerstung, M., MacLean, D., Timmer, J., Fleck, C., and Lenhard, M. (2007). Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev. Cell 13, 843-856.
2. 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.
3. Barrôco, R. M., Peres, A., Droual, A. M., De Veylder, L., Nguyen le, S. L., De Wolf, J., Mironov, V., Peerbolte, R., Beemster, G. T., Inzé, D., Broekaert, W. F., and Frankard, V. (2006). The cyclin-dependent kinase inhibitor Orysa; KRP1 plays an important role in seed development of rice. Plant Physiol. 142, 1053-1064.
4. Beemster, G. T., Fiorani, F., and Inzé, D. (2003). Cell cycle: the key to plant growth control? Trends Plant Sci. 8, 154-158.
5. Beemster, G. T. S., De Veylder, L., Vercruysse, S., West, G., Rombaut, D., Van Hummelen, P., Galichet, A., Gruissem, W., Inzé, D., and Vuylsteke, M. (2005). Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol. 138, 734-743.
6. Boudolf, V., Vlieghe, K., Beemster, G. T. S., Magyar, Z., Torres Acosta, J. A., Maes, S., Van Der Schueren, E., Inzé, D., and De Veylder, L. (2004). The plant-specifc cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endore duplicating cells in Arabidopsis. Plant Cell 16, 2683-2692.
7. Breuer, C., Ishida, T., and Sugimoto, K. (2010). Developmental control of endocycles and cell growth in plants. Curr. Opin. Plant Biol. 13, 654-660.
8. Clay, N. K., and Nelson, T. (2005). The recessive epigenetic swellmap mutation affects the expression of two step II splicing factors required for the transcription of the cell proliferation gene STRUWWELPETER and for the timing of cell cycle arrest in the Arabidopsis leaf. Plant Cell 17, 1994-2008.
9. Cnops, G., Jover-Gil, S., Peters, J. L., Neyt, P., De Block, S., Robles, P., Ponce, M. R., Gerats, T., Micol, J. L., and Van Lijsebettens, M. (2004). The rotunda2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis. J. Exp. Bot. 55, 1529-1539.
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 kinase inhibitors of Arabidopsis. Plant Cell 13, 1653-1668.
11. De Veylder, L., Beeckman, T., Beemster, G. T. S., de Almeida Engler, J., Ormenese, S., Maes, S., Naudts, M., Van Der Schueren, E., Jacqmard, A., Engler, G., and Inzé, D. (2002). Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J. 21, 1360-1368.
12. Delgado-Benarroch, L., Weiss, J., and Egea-Cortines, M. (2009). The mutants compacta ähnlich, nitida and grandi-fora defne developmental compartments and a compensation mechanism in foral development in Antirrhinum majus. J. Plant Res. 122, 559-569.
13. Dewitte, W., Riou-Khamlichi, C., Scofeld, 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. Dewitte, W., Scofeld, S., Alcasabas, A. A., Maughan, S. C., Menges, M., Braun, N., Collins, C., Nieuwland, J., Prinsen, E., Sundaresan, V., and Murray, J. A. H. (2007). Arabidopsis CYCD D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc. Natl. Acad. Sci. U.S.A. 104, 14537-14542.
15. Disch, S., Anastasiou, E., Sharma, V. K., Laux, T., Fletcher, J. C., and Lenhard, M. (2006). The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16, 272-279.
16. 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.
17. Eriksson, S., Stransfeld, L., Adamski, N. M., Breuninger, H., and Lenhard, M. (2010). KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr. Biol. 20, 527-532.
18. Exner, V., Taranto, P., Schönrock, N., Gruissem, W., and Henning, L. (2006). Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 133, 4163-4172.
19. Ferjani, A., Horiguchi, G., Yano, S., and Tsukaya, H. (2007). Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol. 144, 988-999.
20. Fujikura, U., Horiguchi, G., Ponce, M. R., Micol, J. L., and Tsukaya, H. (2009). Coordination of cell proliferation and cell expansion mediated by ribo-some-related processes in the leaves of Arabidopsis thaliana. Plant J. 59, 499-508.
21. Fujikura, U., Horiguchi, G., and Tsukaya, H. (2007a). Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol. 48, 278-286.
22. Fujikura, U., Horiguchi, G., and Tsukaya, H. (2007b). Genetic relationship between angustifolia3 and extra-small sisters highlights novel mechanisms controlling leaf size. Plant Signal. Behav. 2, 378-380.
23. Gonzalez, N., Beemster, G. T. S., and Inzé, D. (2009). David and Goliath: what can the tiny weed Arabidopsis teach us to improve biomass production in crops? Curr. Opin. Plant Biol. 12, 157-164.
24. Haber, A. H. (1962). Non-essentiality of concurrent cell divisions for degree of polarization of leaf growth. I. Studies with radiation-induced mitotic inhibition. Am. J. Bot. 49, 583-589.
25. Hase, Y., Trung, K. H., Matsunaga, T., and Tanaka, A. (2006). A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. Plant J. 46, 317-326.
26. Hemerly, A., Engler Jde, 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.
27. Horiguchi, G., Fujikura, U., Ferjani, A., Ishikawa, N., and Tsukaya, H. (2006). Large-scale histological analysis of leaf mutants using two simple leaf observation methods: identifcation of novel genetic pathways governing the size and shape of leaves. Plant J. 48, 638-644.
28. Horiguchi, G., Gonzalez, N., Beemster, G. T., Inzé, D., and Tsukaya, H. (2009). Impact of segmental chromosomal duplications on leaf size in the grandifolia-D mutants of Arabidopsis thaliana. Plant J. 60, 122-133.
29. Horiguchi, G., Kim, G. T., and Tsukaya, H. (2005). The transcription factor AtGRF5 and the transcription coacti-vator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 43, 68-78.
30. Horiguchi, G., Mollá-Morales, A., Pérez-Pérez, J. M., Kojima, K., Robles, P., Ponce, M. R., Micol, J. L., and Tsukaya, H. (2011). Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J. 65, 724-736.
31. Hu, Y., Poh, H. M., and Chua, N.-H. (2006). The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J. 47, 1-9.
32. Ichihashi, Y., Horiguchi, G., Gleissberg, S., and Tsukaya, H. (2010). The bHLH transcription factor SPATULA controls fnal leaf size in Arabidopsis thaliana. Plant Cell Physiol. 51, 252-261.
33. Inzé, D., and De Veylder, L. (2006). Cell cycle regulation in plant development. Annu. Rev. Genet. 40, 77-105.
34. 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.
35. Kang, J., Mizukami, Y., Wang, H., Fowke, L., and Dengler, N. G. (2007). Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226, 1207-1218.
36. Kaplan, D. R. (2001). Fundamental concepts of leaf morphology and morphogenesis: a contribution to the interpretation of molecular genetic mutants. Int. J. Plant Sci. 162, 465-474.
37. Kawade, K., Horiguchi, G., and Tsukaya, H. (2010). Non-cell-autonomously coordinated organ size regulation in leaf development. Development 137, 4221-4227.
38. Kazama, T., Ichihashi, Y., Murata, S., and Tsukaya, H. (2010). The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thali-ana. Plant Cell Physiol. 51, 1046-1054.
39. Kim, J. H., and Kende, H. (2004). A tran-scriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 13374-13379.
40. Krizek, B. (2009). Making bigger plants: key regulators of fnal organ size. Cu r r. Opin. Plant Biol. 12, 17-22.
41. Li, Y. H., Zheng, L. Y., Corke, F., Smith, C., and Bevan, M. W. (2008). Control of fnal seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 22, 1331-1336.
42. Liu, D., Song, Y., Chen, Z., and Yu, D. (2009). Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol. Plant. 136, 223-236.
43. Melaragno, J. E., Mehrotra, B., and Coleman, A. W. (1993). Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5, 1661-1668.
44. Micol, J. L. (2009). Leaf development: time to turn over a new leaf? Curr. Opin. Plant Biol. 12, 9-16.
45. Mizukami, Y., and Fischer, R. L. (2000). Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogen-esis. Proc. Natl. Acad. Sci. U.S.A. 97, 942-947.
46. Narita, N. N., Moore, S., Horiguchi, G., Kubo, M., Demura, T., Fukuda, H., Goodrich, J., and Tsukaya, H. (2004). Overexpression of a novel small pep-tide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J. 38, 699-713.
47. Radziejwoski, A., Vlieghe, K., Lammens, T., Berckmans, B., Maes, S., Jansen, M. A., Knappe, C., Albert, A., Seidlitz, H. K., Bahnweg, G., Inzé, D., and De Veylder, L. (2011). Atypical E2F activity coordinates PHR1 photolyase gene transcription with endoreduplication onset. EMBO J. 30, 355-363.
48. Ramirez-Parra, E., and Gutierrez, C. (2007). E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activate gene expression by changing the epigenetic status. Plant Physiol. 144, 105-120.
49. Rizzini, L., Favory, J. J., Cloix, C., Faggionato, D., O'Hara, A., Kaiserli, E., Baumeister, R., Schäfer, E., Nagy, F., Jenkins, G. I., and Ulm, R. (2011). Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103-106.
50. Rodriguez, R. E., Mecchia, M. A., Debernardi, J. M., Schommer, C., Weigel, D., and Palatnik, J. F. (2010). Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137, 103-112.
51. Strabala, T. J., O'Donnell, P. J., Smit, A.-M., Ampomah-Dwamena, C., Martin, E. J., Netzler, N., Nieuwenhuizen, N. J., Quinn, B. D., Foote, H. C. C., and Hudson, K. R. (2006). Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CAVATA3/ESR domain. Plant Physiol. 140, 1331-1344.
52. Szécsi, J., Joly, C., Bordji, K., Varaud, E., Cock, J. M., Dumas, C., and Bendahmane, M. (2006). BIGPETALp, bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J. 25, 3912-3920.
53. Takahashi, N., Lammens, T., Boudolf, V., Maes, S., Yoshizumi, T., De Jaeger, G., Witters, E., Inzé, D., and De Veylder, L. (2008). The DNA replication checkpoint aids survival of plants defcient in the novel replisome factor ETG1. EMBO J. 27, 1840-1851.
54. Traas, J., Hülskamp, M., Gendreau, E., and Höfte, H. (1998). Endoreduplication and development: rule without dividing? Curr. Opin. Plant Biol. 1, 498-503.
55. 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.
56. Tsukaya, H. (2008). Controlling size in multicellular organs: focus on the leaf. PLoS Biol. 6, e174. doi: 10.1371/ journal.pbio.0060174
57. 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.
58. Usami, T., Horiguchi, G., Yano, S., and Tsukaya, H. (2009). The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136, 955-964.
59. Verkest, A., Manes, C.-L., Vercruysse, S., Maes, S., Van Der Schueren, E., Beeckman, T., Genschik, P., Kuiper, M., Inzé, D., and De Veylder, L. (2005). The cyclin-dependent kinase inhibitor KRP2 controls the onset of endore-duplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17, 1723-1736.
60. 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.
61. Wang, Y., Henriksson, E., Söderman, E., Henriksson, K. N., Sundberg, E., and Engström, P. (2003). The Arabidopsis homeobox gene, ATHB16, regulates leaf development and sensitivity to photoperiod in Arabidopsis. Dev. Biol. 264, 228-239.
62. Wargent, J. J., Gegas, V. C., Jenkins, G. I., Doonan, J. H., and Paul, N. D. (2009). UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation. New Phytol. 183, 315-326.
63. White, D. W. (2006). PEAPOD regulates lamina size and curvature in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 13238-13243.
64. Wu, C.-Y., Rolfe, P. A., Gifford, D. K., and Fink, G. R. (2010). Control of transcription by cell size. PLoS Biol. 8, e1000523. doi: 10.1371/journal. pbio.1000523
65. Yuan, Z., Luo, D., Li, G., Yao, X., Wang, H., Zeng, M., Huang, H., and Cui, X. (2010). Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J. 64, 331-342.