Brassinosteroid production and signaling differentially control cell division and expansion in the leaf

New Phytologist

Volumn 197, Issue 2, 2013, Pages 490-502

  Zhiponova, Miroslava K ^a,b   Vanhoutte, Isabelle ^a,b   Boudolf, Véronique ^a,b   Betti, Camilla ^a,b   Dhondt, Stijn ^a,b   Coppens, Frederik ^a,b   Mylle, Evelien ^a,b   Maes, Sara ^a,b   González García, Mary Paz ^c   Caño Delgado, Ana I ^c   Inzé, Dirk ^a,b   Beemster, Gerrit T S ^d   De Veylder, Lieven ^a,b   Russinova, Eugenia ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c CSIC   (Spain)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Arabidopsis; Brassinosteroids; Cell division; cpd; Leaf

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; BRI1 PROTEIN, ARABIDOPSIS; PROTEIN KINASE;

DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC MARKER; GROWTH; HORMONE; KINEMATICS; LEAF; MUTATION; PROTEIN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL COUNT; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL SIZE; CYTOLOGY; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; MUTATION; PHENOTYPE; PLANT LEAF; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; CELL COUNT; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL SIZE; MITOSIS; MUTATION; PHENOTYPE; PLANT LEAVES; PROTEIN KINASES; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

EID: 84871279647     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12036     Document Type: Article

References (75)

1. Abràmoff MD, Magalhães PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics International 11: 36-42.
2. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GTS, Genschik P. 2009. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Current Biology 19: 1188-1193.
3. Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GTS et al. 2012. Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Developmental Cell 22: 64-78.
4. Azpiroz R, Wu Y, LoCascio JC, Feldmann KA. 1998. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10: 219-230.
5. Azzi L, Meijer L, Ostvold A-C, Lew J, Wang JH. 1994. Purification of a 15-kDa cdk4- and cdk5-binding protein. Journal of Biological Chemistry 269: 13279-13288.
6. Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z. 2004. Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiology 134: 1624-1631.
7. Beemster GTS, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M. 2005. Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiology 138: 734-743.
8. Beuchat J, Scacchi E, Tarkowska D, Ragni L, Strnad M, Hardtke CS. 2010. BRX promotes Arabidopsis shoot growth. New Phytologist 188: 23-29.
9. Bögre L, Magyar Z, López-Juez E. 2008. New clues to organ size control in plants. Genome Biology 9: 226.
10. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng J-C, Nam KH, Li J, Chory J. 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351.
11. Cheon J, Park S-Y, Schulz B, Choe S. 2010. Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC Plant Biology 10: 270.
12. Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA 1998. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10: 231-243.
13. Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S, Tanaka A, Yoshida S et al. 1999. The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiology 119: 897-907.
14. Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA. 2001. Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant Journal 26: 573-582.
15. Chory J, Nagpal P, Peto CA. 1991. Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3: 445-459.
16. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
17. Clouse SD, Langford M, McMorris TC. 1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiology 111: 671-678.
18. Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P. 1999. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant Journal 20: 503-508.
19. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R et al. 2008. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322: 594-597.
20. De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D. 2001. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653-1667.
21. De Veylder L, Larkin JC, Schnittger A. 2011. Molecular control and function of endoreplication in development and physiology. Trends in Plant Science 16: 624-634.
22. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JAH. 2003. Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15: 79-92.
23. Dhondt S, Van Haerenborgh D, Van Cauwenbergh C, Merks RMH, Philips W, Beemster GTS, Inzé D. 2012. Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis. Plant Journal 69: 553-563.
24. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. 1999. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Developmental Biology 215: 407-419.
25. Efroni I, Eshed Y, Lifschitz E. 2010. Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22: 1019-1032.
26. Eloy NB, De Freitas Lima M, Van Damme D, Vanhaeren H, Gonzalez N, De Milde L, Hemerly AS, Beemster GTS, Inzé D, Ferreira PCG. 2011. The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant Journal 68: 351-363.
27. Fiorani F, Beemster GTS. 2006. Quantitative analyses of cell division in plants. Plant Molecular Biology 60: 963-979.
28. Friedrichsen DM, Joazeiro CAP, Li J, Hunter T, Chory J. 2000. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiology 123: 1247-1255.
29. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
30. Fujioka S, Li J, Choi Y-H, Seto H, Takatsuto S, Noguchi T, Watanabe T, Kuriyama H, Yokota T, Chory J et al. 1997. The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9: 1951-1962.
31. Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, Dhondt S, Van Daele T, De Milde L, Weigel D, Kamiya Y et al. 2010. Increased leaf size: different means to an end. Plant Physiology 153: 1261-1279.
32. Gonzalez N, Vanhaeren H, Inzé D. 2012. Leaf size control: complex coordination of cell division and expansion. Trends in Plant Science 17: 332-340.
33. González-García MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S, Russinova E, Caño-Delgado AI. 2011. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138: 849-859.
34. Gudesblat GE, Russinova E. 2011. Plants grow on brassinosteroids. Current Opinion in Plant Biology 14: 530-537.
35. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S. 2011. Brassinosteroid perception in the epidermis controls root meristem size. Development 138: 839-848.
36. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8: R19.
37. Hu Y, Bao F, Li J. 2000. Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant Journal 24: 693-701.
38. Ibañes M, Fàbregas N, Chory J, Caño-Delgado AI. 2009. Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proceedings of the National Academy of Sciences of the United States of America 106: 13630-13635.
39. Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T. 1996. Genetic evidence for an essential role of brassinosteroids in plant development. Plant Journal 9: 701-713.
40. Kazama T, Ichihashi Y, Murata S, 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 thaliana. Plant and Cell Physiology 51: 1046-1054.
41. Li J, Chory J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
42. Li J, Nam KH, Vafeados D, Chory J. 2001. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiology 127: 14-22.
43. Marrocco K, Thomann A, Parmentier Y, Genschik P, Criqui MC. 2009. The APC/C E3 ligase remains active in most post-mitotic Arabidopsis cells and is required for proper vasculature development and organization. Development 136: 1475-1485.
44. Miyazawa Y, Nakajima N, Abe T, Sakai A, Fujioka S, Kawano S, Kuroiwa T, Yoshida S. 2003. Activation of cell proliferation by brassinolide application in tobacco BY-2 cells: effects of brassinolide on cell multiplication, cell-cycle-related gene expression, and organellar DNA contents. Journal of Experimental Botany 54: 2669-2678.
45. Nakajima N, Shida A, Toyama S. 1996. Effects of brassinosteroid on cell division and colony formation of Chinese cabbage mesophyll protoplasts. Japanese Journal of Crop Science 65: 125-130.
46. Nakamura A, Fujioka S, Sunohara H, Kamiya N, Hong Z, Inukai Y, Miura K, Takatsuto S, Yoshida S, Ueguchi-Tanaka M et al. 2006. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiology 140: 580-590.
47. Nakamura M, Naoi K, Shoji T, Hashimoto T. 2004. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant and Cell Physiology 45: 1330-1334.
48. Nakaya M, Tsukaya H, Murakami N, Kato M. 2002. Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant and Cell Physiology 43: 239-244.
49. Oh M-H, Clouse SD. 1998. Brassinolide affects the rate of cell division in isolated leaf protoplasts of Petunia hybrida. Plant Cell Reports 17: 921-924.
50. Oh M-H, Sun J, Oh DH, Zielinski RE, Clouse SD, Huber SC. 2011. Enhancing Arabidopsis leaf growth by engineering the BRASSINOSTEROID INSENSITIVE 1 receptor kinase. Plant Physiology 157: 120-131.
51. Ohashi-Ito K, Fukuda H. 2003. HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant and Cell Physiology 44: 1350-1358.
52. Pérez-Pérez JM, Serralbo O, Vanstraelen M, González C, Criqui M-C, Genschik P, Kondorosi E, Scheres B. 2008. Specialization of CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C). Plant Journal 53: 78-89.
53. Reinhardt B, Hänggi E, Müller S, Bauch M, Wyrzykowska J, Kerstetter R, Poethig S, Fleming AJ. 2007. Restoration of DWF4 expression to the leaf margin of a dwf4 mutant is sufficient to restore leaf shape but not size: the role of the margin in leaf development. Plant Journal 52: 1094-1104.
54. Savaldi-Goldstein S, Peto C, Chory J. 2007. The epidermis both drives and restricts plant shoot growth. Nature 446: 199-202.
55. Scarpella E, Marcos D, Friml J, Berleth T. 2006. Control of leaf vascular patterning by polar auxin transport. Genes and Development 20: 1015-1027.
56. Schnittger A, Schöbinger U, Stierhof Y-D, Hülskamp M. 2002. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Current Biology 12: 415-420.
57. Serralbo O, Pérez-Pérez JM, Heidstra R, Scheres B. 2006. Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog. Proceedings of the National Academy of Sciences of the United States of America 103: 13250-13255.
58. Skirycz A, Inzé D. 2010. More from less: plant growth under limited water. Current Opinion in Biotechnology 21: 197-203.
59. Snustad DP, Haas NA, Kopczak SD, Silflow CD. 1992. The small genome of Arabidopsis contains at least nine expressed ß-tubulin genes. Plant Cell 4: 549-556.
60. Sun Y, Fan X-Y, Cao D-M, Tang W, He K, Zhu J-Y, He J-X, Bai M-Y, Zhu S, Oh E et al. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19: 765-777.
61. Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171-182.
62. 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. International Review of Cytology 217: 1-39.
63. Tsukaya H. 2005. Leaf shape: genetic controls and environmental factors. International Journal of Developmental Biology 49: 547-555.
64. Tsukaya H. 2006. Mechanism of leaf-shape determination. Annual Review of Plant Biology 57: 477-496.
65. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. 1997. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
66. Van Esse GW, Westphal AH, Surendran RP, Albrecht C, van Veen B, Borst JW, de Vries SC. 2011. Quantification of the brassinosteroid insensitive1 receptor in planta. Plant Physiology 156: 1691-1700.
67. Vanneste S, Coppens F, Lee E, Donner TJ, Xie Z, Van Isterdael G, Dhondt S, De Winter F, De Rybel B, Vuylsteke M et al. 2011. Developmental regulation of CYCA2s contributes to tissue-specific proliferation in Arabidopsis. EMBO Journal 30: 3430-3441.
68. Völker A, Stierhof Y-D, Jürgens G. 2001. Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. Journal of Cell Science 114: 3001-3012.
69. Wang Z-Y, Seto H, Fujioka S, Yoshida S, Chory J. 2001. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380-383.
70. Weingartner M, Criqui M-C, Mészáros T, Binarova P, Schmit A-C, Helfer A, Derevier A, Erhardt M, Bögre L, Genschik P. 2004. Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast. Plant Cell 16: 643-657.
71. Wenzel CL, Schuetz M, Yu Q, Mattsson J. 2007. Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant Journal 49: 387-398.
72. Wu S, Scheible W-R, Schindelasch D, Van Den Daele H, De Veylder L, Baskin TI. 2010. A conditional mutation in Arabidopsis thaliana separase induces chromosome non-disjunction, aberrant morphogenesis and cyclin B1;1 stability. Development 137: 953-961.
73. Yin Y, Wang Z-Y, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J. 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181-191.
74. Yoshizumi T, Nagata N, Shimada H, Matsui M. 1999. An Arabidopsis cell cycle- dependent kinase-related gene, CDC2b, plays a role in regulating seedling growth in darkness. Plant Cell 11: 1883-1895.
75. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P et al. 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant Journal 65: 634-646.