Home LiteratureArticle Details
PMID: 23213257 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 109 ·No. 51 ·2012-12-18 ·Pages 21152-7

Gendron JM, Liu JS, Fan M, Bai MY, Wenkel S, Springer PS, Barton MK, Wang ZY

Abstract

Spatiotemporal control of the formation of organ primordia and organ boundaries from the stem cell niche in the shoot apical meristem (SAM) determines the patterning and architecture of plants, but the underlying signaling mechanisms remain poorly understood. Here we show that brassinosteroids (BRs) play a key role in organ boundary formation by repressing organ boundary identity genes. BR-hypersensitive mutants display organ-fusion phenotypes, whereas BR-insensitive mutants show enhanced organ boundaries. The BR-activated transcription factor BZR1 directly represses the cup-shaped cotyledon (CUC) family of organ boundary identity genes. In WT plants, BZR1 accumulates at high levels in the nuclei of central meristem and organ primordia but at a low level in organ boundary cells to allow CUC gene expression. Activation of BR signaling represses CUC gene expression and causes organ fusion phenotypes. This study uncovers a role for BR in the spatiotemporal control of organ boundary formation and morphogenesis in the SAM.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/metabolism Brassinosteroids/metabolism Cell Nucleus/metabolism Chromatin Immunoprecipitation Gene Expression Regulation, Plant Genes, Plant Meristem/physiology Microscopy, Confocal/methods Microscopy, Electron, Scanning/methods Mutation Phenotype Plant Shoots/metabolism Signal Transduction
Chemicals
Arabidopsis Proteins Brassinosteroids
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Gendron Joshua M
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
Liu Jiang-Shu
Fan Min
Bai Ming-Yi
Wenkel Stephan
Springer Patricia S
Barton M Kathryn
Wang Zhi-Yong
References (48)
48 references, click to expand
  1. Structural basis of steroid hormone perception by the receptor kinase BRI1.
    Nature. 2011 Jun 12;474(7352):467-71 PMID: 21666665
  2. Progesterone induces adult mammary stem cell expansion.
    Nature. 2010 Jun 10;465(7299):803-7 PMID: 20445538
  3. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis.
    Cell. 1996 Apr 19;85(2):171-82 PMID: 8612270
  4. Plant and animal stem cells: conceptually similar, molecularly distinct?
    Trends Cell Biol. 2004 Nov;14(11):605-11 PMID: 15519849
  5. Molecular mechanisms of steroid hormone signaling in plants.
    Annu Rev Cell Dev Biol. 2005;21:177-201 PMID: 16212492
  6. Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex.
    Plant Mol Biol. 2006 Apr;60(6):915-28 PMID: 16724261
  7. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint.
    Plant Cell. 2000 Sep;12(9):1591-606 PMID: 11006334
  8. A role for brassinosteroids in light-dependent development of Arabidopsis.
    Science. 1996 Apr 19;272(5260):398-401 PMID: 8602526
  9. The dynamic plant stem cell niches.
    Curr Opin Plant Biol. 2007 Dec;10(6):639-44 PMID: 17692560
  10. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis.
    Plant Cell. 2009 Dec;21(12):3767-80 PMID: 20009022
  11. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots.
    Development. 2011 Mar;138(5):849-59 PMID: 21270057
  12. Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries.
    Proc Natl Acad Sci U S A. 2012 Dec 18;109(51):21146-51 PMID: 23213252
  13. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis.
    Nat Cell Biol. 2012 Aug;14(8):810-7 PMID: 22820377
  14. Genetic control of shoot organ boundaries.
    Curr Opin Plant Biol. 2006 Feb;9(1):72-7 PMID: 16337829
  15. Structural insight into brassinosteroid perception by BRI1.
    Nature. 2011 Jun 12;474(7352):472-6 PMID: 21666666
  16. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis.
    Dev Cell. 2010 Nov 16;19(5):765-77 PMID: 21074725
  17. The lateral organ boundaries gene defines a novel, plant-specific gene family.
    Plant Physiol. 2002 Jun;129(2):747-61 PMID: 12068116
  18. A role for chromatin remodeling in regulation of CUC gene expression in the Arabidopsis cotyledon boundary.
    Development. 2006 Aug;133(16):3223-30 PMID: 16854978
  19. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation.
    Plant Cell. 2006 Nov;18(11):2946-57 PMID: 17122068
  20. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis.
    Dev Cell. 2007 Aug;13(2):177-89 PMID: 17681130
  21. The meristem-to-organ boundary: more than an extremity of anything.
    Curr Opin Genet Dev. 2008 Aug;18(4):287-94 PMID: 18590819
  22. Control of mammary stem cell function by steroid hormone signalling.
    Nature. 2010 Jun 10;465(7299):798-802 PMID: 20383121
  23. Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo.
    Development. 2002 Sep;129(17):3965-74 PMID: 12163400
  24. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis.
    Development. 2004 Oct;131(20):5021-30 PMID: 15371311
  25. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis.
    Development. 2009 Jul;136(14):2423-32 PMID: 19542355
  26. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.
    Curr Biol. 2005 Nov 8;15(21):1899-911 PMID: 16271866
  27. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):10185-90 PMID: 12114546
  28. Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis.
    Plant J. 2011 May;66(4):564-78 PMID: 21284753
  29. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis.
    Dev Cell. 2002 Apr;2(4):505-13 PMID: 11970900
  30. Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels.
    Plant Physiol. 2004 Aug;135(4):2196-206 PMID: 15299131
  31. Brassinosteroid signal transduction from receptor kinases to transcription factors.
    Annu Rev Plant Biol. 2010;61:681-704 PMID: 20192752
  32. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes.
    Development. 1999 Apr;126(8):1563-70 PMID: 10079219
  33. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice.
    Plant Physiol. 2006 Feb;140(2):580-90 PMID: 16407447
  34. Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction.
    BMC Plant Biol. 2010 Dec 09;10:270 PMID: 21143877
  35. Multiple mechanisms modulate brassinosteroid signaling.
    Curr Opin Plant Biol. 2007 Oct;10(5):436-41 PMID: 17904409
  36. Tomato BRASSINOSTEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling.
    Plant Cell. 2007 May;19(5):1709-17 PMID: 17513502
  37. The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells.
    EMBO J. 2010 Aug 18;29(16):2700-14 PMID: 20717140
  38. Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles.
    Proc Natl Acad Sci U S A. 2009 Aug 11;106(32):13630-5 PMID: 19666540
  39. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1.
    Nat Cell Biol. 2011 Feb;13(2):124-31 PMID: 21258370
  40. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves.
    Development. 2009 Mar;136(5):823-32 PMID: 19176589
  41. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis.
    Plant Cell. 2006 Nov;18(11):2929-45 PMID: 17098808
  42. BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:427-451 PMID: 15012241
  43. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses.
    Science. 2005 Mar 11;307(5715):1634-8 PMID: 15681342
  44. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
    Plant Cell. 1997 Jun;9(6):841-57 PMID: 9212461
  45. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway.
    Nature. 2012 Feb 05;482(7385):419-22 PMID: 22307275
  46. Brassinosteroid perception in the epidermis controls root meristem size.
    Development. 2011 Mar;138(5):839-48 PMID: 21270053
  47. Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis.
    Dev Cell. 2010 Dec 14;19(6):872-83 PMID: 21145502
  48. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses.
    Nat Cell Biol. 2012 Aug;14(8):802-9 PMID: 22820378
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.1210799110
Published
2012-12-18
Epub
2012-00-04
Pages
21152-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3529081
Subset
IM
Grants
NIGMS NIH HHS · R01 GM066258 · United States
Corrections
CommentIn
PMID: 23384602
CommentIn
PMID: 23428325
External Links
PubMed source DOI: 10.1073/pnas.1210799110 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2