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PMID: 21504914 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Auxin, cytokinin and the control of shoot branching.

Annals of botany ·Vol. 107 ·No. 7 ·2011-05-00 ·Pages 1203-12

Müller D, Leyser O

Abstract

It has been known for many decades that auxin inhibits the activation of axillary buds, and hence shoot branching, while cytokinin has the opposite effect. However, the modes of action of these two hormones in branching control is still a matter of debate, and their mechanisms of interaction are equally unresolved. Here we review the evidence for various hypotheses that have been put forward to explain how auxin and cytokinin influence axillary bud activity. In particular we discuss the roles of auxin and cytokinin in regulating each other's synthesis, the cell cycle, meristem function and auxin transport, each of which could affect branching. These different mechanisms have implications for the main site of hormone action, ranging from systemic action throughout the plant, to local action at the node or in the bud meristem or leaves. The alternative models have specific predictions, and our increasing understanding of the molecular basis for hormone transport and signalling, cell cycle control and meristem biology is providing new tools to enable these predictions to be tested.

MeSH Terms
Cytokinins/metabolism Indoleacetic Acids/metabolism Meristem/growth & development,metabolism Models, Biological Plant Shoots/growth & development,metabolism
Chemicals
Cytokinins Indoleacetic Acids
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Müller Dörte
Department of Biology, University of York, York, UK.
Leyser Ottoline
References (78)
78 references, click to expand
  1. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction.
    Plant Cell. 2010 Sep;22(9):2956-69 PMID: 20823193
  2. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities.
    Curr Biol. 2005 Sep 6;15(17):1560-5 PMID: 16139211
  3. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1.
    Nature. 2004 Aug 26;430(7003):1031-4 PMID: 15329722
  4. Cell cycle regulation during growth-dormancy cycles in pea axillary buds.
    Plant Mol Biol. 1995 Oct;29(2):255-65 PMID: 7579177
  5. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression.
    Development. 2005 Oct;132(20):4521-31 PMID: 16192309
  6. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-Zeatin.
    J Biol Chem. 2004 Oct 1;279(40):41866-72 PMID: 15280363
  7. The hormonal regulation of axillary bud growth in Arabidopsis.
    Plant J. 2000 Oct;24(2):159-69 PMID: 11069691
  8. SOME RESPONSES OF PLANTS TO 2,3,5-TRIIODOBENZOIC ACID.
    Plant Physiol. 1949 Apr;24(2):195-206 PMID: 16654211
  9. FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice.
    Plant Cell Physiol. 2010 Jul;51(7):1127-35 PMID: 20547591
  10. Arabidopsis KNOXI proteins activate cytokinin biosynthesis.
    Curr Biol. 2005 Sep 6;15(17):1566-71 PMID: 16139212
  11. The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport.
    Curr Biol. 2006 Mar 21;16(6):553-63 PMID: 16546078
  12. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice.
    Plant J. 2007 Sep;51(6):1019-29 PMID: 17655651
  13. Direct control of shoot meristem activity by a cytokinin-activating enzyme.
    Nature. 2007 Feb 8;445(7128):652-5 PMID: 17287810
  14. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth.
    Plant J. 2001 Nov;28(4):465-74 PMID: 11737783
  15. Integrating cellular and organismic aspects of vascular differentiation.
    Plant Cell Physiol. 2000 Jun;41(6):649-56 PMID: 10945333
  16. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate.
    Plant J. 2004 Jan;37(1):128-38 PMID: 14675438
  17. Ectopic expression of Arabidopsis CYCD2 and CYCD3 in tobacco has distinct effects on the structural organization of the shoot apical meristem.
    J Exp Bot. 2005 Jan;56(409):123-34 PMID: 15501911
  18. Analysis of cycles of dormancy and growth in pea axillary buds based on mRNA accumulation patterns of cell cycle-related genes.
    Plant Cell Physiol. 1998 Mar;39(3):255-62 PMID: 9588023
  19. Genetic regulation of branching morphogenesis: lessons learned from loss-of-function phenotypes.
    Pediatr Res. 2003 Oct;54(4):433-8 PMID: 12904600
  20. The evolution of apical dominance in maize.
    Nature. 1997 Apr 3;386(6624):485-8 PMID: 9087405
  21. The OsTB1 gene negatively regulates lateral branching in rice.
    Plant J. 2003 Feb;33(3):513-20 PMID: 12581309
  22. 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
  23. Stimulatory effect of cytokinins and interaction with IAA on the release of lateral buds of pea plants from apical dominance.
    J Plant Physiol. 2003 Sep;160(9):1059-63 PMID: 14593807
  24. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds.
    Plant Cell. 2007 Feb;19(2):458-72 PMID: 17307924
  25. Hormonal control of the shoot stem-cell niche.
    Nature. 2010 Jun 24;465(7301):1089-92 PMID: 20577215
  26. Auxin and kinetin interaction in apical dominance.
    Science. 1966 Jan 28;151(3709):468-9 PMID: 17798523
  27. Regulation of cytokinin biosynthesis, compartmentalization and translocation.
    J Exp Bot. 2008;59(1):75-83 PMID: 17872922
  28. Feedback regulation of xylem cytokinin content is conserved in pea and Arabidopsis.
    Plant Physiol. 2007 Mar;143(3):1418-28 PMID: 17277096
  29. PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene.
    Plant Cell. 1997 Sep;9(9):1607-19 PMID: 9338963
  30. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance.
    Plant J. 2006 Mar;45(6):1028-36 PMID: 16507092
  31. Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis.
    Plant Physiol. 2009 May;150(1):482-93 PMID: 19321710
  32. Expression of a ribosomal protein gene in axillary buds of pea seedlings.
    Plant Physiol. 1992 Nov;100(3):1494-502 PMID: 16653149
  33. Overexpression of the maize Teosinte Branched1 gene in wheat suppresses tiller development.
    Plant Cell Rep. 2008 Jul;27(7):1217-25 PMID: 18392625
  34. Regulation of plant growth by cytokinin.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10487-92 PMID: 11504909
  35. Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development.
    Proc Natl Acad Sci U S A. 2004 May 25;101(21):8039-44 PMID: 15146070
  36. TCP genes: a family snapshot ten years later.
    Trends Plant Sci. 2010 Jan;15(1):31-9 PMID: 19963426
  37. Cytokinin activation of Arabidopsis cell division through a D-type cyclin.
    Science. 1999 Mar 5;283(5407):1541-4 PMID: 10066178
  38. Strigolactones enhance competition between shoot branches by dampening auxin transport.
    Development. 2010 Sep 1;137(17):2905-13 PMID: 20667910
  39. Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):757-66 PMID: 15908603
  40. Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals.
    Plant Physiol. 2006 Mar;140(3):1109-17 PMID: 16443694
  41. Vegetative axillary bud dormancy induced by shade and defoliation signals in the grasses.
    Plant Signal Behav. 2010 Mar;5(3):317-9 PMID: 20200487
  42. Arabidopsis TCP20 links regulation of growth and cell division control pathways.
    Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12978-83 PMID: 16123132
  43. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase.
    Plant Cell. 2001 Sep;13(9):2115-25 PMID: 11549767
  44. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis.
    Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16598-603 PMID: 17062755
  45. Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants.
    Plant J. 1997 Aug;12(2):401-15 PMID: 9301091
  46. Experimental cytology of the shoot apical cells during vegetative growth and flowering.
    Int Rev Cytol. 1967;21:203-351 PMID: 5338240
  47. Cytokinins are central regulators of cambial activity.
    Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):20027-31 PMID: 19074290
  48. Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice.
    Plant Physiol. 2006 Sep;142(1):54-62 PMID: 16861569
  49. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis.
    Plant Cell. 2009 Oct;21(10):3152-69 PMID: 19837870
  50. Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells.
    Plant J. 2003 Mar;33(6):957-66 PMID: 12631321
  51. The TCP domain: a motif found in proteins regulating plant growth and development.
    Plant J. 1999 Apr;18(2):215-22 PMID: 10363373
  52. Suppression of sorghum axillary bud outgrowth by shade, phyB and defoliation signalling pathways.
    Plant Cell Environ. 2010 Jan;33(1):48-58 PMID: 19843258
  53. Metabolism and long-distance translocation of cytokinins.
    J Integr Plant Biol. 2010 Jan;52(1):53-60 PMID: 20074140
  54. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling.
    Plant Cell. 2004 Mar;16(3):658-71 PMID: 14973166
  55. Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition.
    J Exp Bot. 2003 Nov;54(392):2511-7 PMID: 14512385
  56. Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1.
    Plant Physiol. 1998 Feb;116(2):471-6 PMID: 9489007
  57. A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem.
    Dev Biol. 2009 Dec 1;336(1):1-9 PMID: 19782675
  58. A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription.
    Plant Cell. 1998 Mar;10(3):331-41 PMID: 9501108
  59. Functional domains in plant shoot meristems.
    Bioessays. 2001 Feb;23(2):134-41 PMID: 11169586
  60. Control of bud activation by an auxin transport switch.
    Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17431-6 PMID: 19805140
  61. Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth.
    Plant J. 2011 Feb;65(4):571-7 PMID: 21219506
  62. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.
    Nature. 2005 Jan 6;433(7021):39-44 PMID: 15635403
  63. Studies on the Growth Hormone of Plants: III. The Inhibiting Action of the Growth Substance on Bud Development.
    Proc Natl Acad Sci U S A. 1933 Jul;19(7):714-6 PMID: 16577553
  64. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14537-42 PMID: 17726100
  65. Two of three promoter elements identified in a rice gene for proliferating cell nuclear antigen are essential for meristematic tissue-specific expression.
    Plant J. 1995 Jun;7(6):877-86 PMID: 7599648
  66. A role for flavin monooxygenase-like enzymes in auxin biosynthesis.
    Science. 2001 Jan 12;291(5502):306-9 PMID: 11209081
  67. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators.
    Nature. 2005 Dec 22;438(7071):1172-5 PMID: 16372013
  68. In planta functions of the Arabidopsis cytokinin receptor family.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8821-6 PMID: 15166290
  69. Auxin acts in xylem-associated or medullary cells to mediate apical dominance.
    Plant Cell. 2003 Feb;15(2):495-507 PMID: 12566587
  70. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans.
    Curr Biol. 2002 Sep 17;12(18):1557-65 PMID: 12372247
  71. Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte.
    Genetics. 2002 Dec;162(4):1927-35 PMID: 12524360
  72. Transport of exogenous auxin in two-branched dwarf pea seedlings (Pisum sativum L.) : Some implications for polarity and apical dominance.
    Planta. 1977 Jan;136(1):91-6 PMID: 24420232
  73. Arabidopsis Teosinte Branched1-like 1 regulates axillary bud outgrowth and is homologous to monocot Teosinte Branched1.
    Plant Cell Physiol. 2007 May;48(5):667-77 PMID: 17452340
  74. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.
    Plant Cell. 2003 Nov;15(11):2532-50 PMID: 14555694
  75. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem.
    Genes Dev. 2001 Mar 1;15(5):581-90 PMID: 11238378
  76. Hormone mediated regulation of the shoot apical meristem.
    Plant Mol Biol. 2009 Mar;69(4):397-408 PMID: 18797999
  77. The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene.
    Plant Physiol. 2000 Apr;122(4):1137-48 PMID: 10759509
  78. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche.
    Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4941-6 PMID: 19258454
Article Info
Journal
Annals of botany
Abbr.
Ann Bot
ISSN
1095-8290
Published
2011-05-00
Epub
2011-00-18
Pages
1203-12
Language
English
Region
England
NLM ID
0372347
PMCID
PMC3091808
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/E024750/1 · United Kingdom
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