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PMID: 12417698 Published · ppublish English Journal Article

Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression.

The Plant cell ·Vol. 14 ·No. 11 ·2002-11-00 ·Pages 2745-60

Tao LZ, Cheung AY, Wu HM

Abstract

The auxin indole-3-acetic acid is a key plant hormone essential for a broad range of growth and developmental processes. Here, we show that auxin activates Rac-like GTPases (referred to as Rac/Rop GTPases), and they in turn stimulate auxin-responsive gene expression. In particular, we show that overexpressing a wild-type tobacco Rac/Rop GTPase, NtRac1, and its constitutively active mutant form activates auxin-responsive gene expression. On the other hand, overexpressing dominant-negative NtRac1 and Rac-negative regulators, or reducing the endogenous NtRac1 level, suppresses auxin-induced gene expression. Furthermore, overexpression of NtRac1 activity or suppression of its expression in transgenic seedlings induces phenotypes that are similar to auxin-related defects. Together, our results show that a subset of plant Rac/Rop GTPases functions in mediating the auxin signal to downstream responsive genes.

MeSH Terms
Arabidopsis Proteins/genetics,metabolism Cell Membrane/drug effects Gene Expression Regulation, Enzymologic/drug effects Gene Expression Regulation, Plant/drug effects Indoleacetic Acids/pharmacology Molecular Sequence Data Phenotype Plants, Genetically Modified Signal Transduction/drug effects Tobacco/enzymology,genetics,growth & development rac GTP-Binding Proteins/genetics,metabolism rho GTP-Binding Proteins/genetics,metabolism
Chemicals
Arabidopsis Proteins Indoleacetic Acids indoleacetic acid RopGAP4 protein, Arabidopsis rac GTP-Binding Proteins rho GTP-Binding Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tao Li-zhen
Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003, USA.
Cheung Alice Y
Wu Hen-ming
References (87)
87 references, click to expand
  1. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings.
    Plant J. 2000 Dec;24(6):785-96 PMID: 11135112
  2. Molecular cloning and expression of the early auxin-responsive Aux/IAA gene family in Nicotiana tabacum.
    Plant Cell Physiol. 1998 Oct;39(10):993-1002 PMID: 9871362
  3. Polar auxin transport: controlling where and how much.
    Trends Plant Sci. 2001 Nov;6(11):535-42 PMID: 11701382
  4. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development.
    EMBO J. 1998 Mar 2;17(5):1405-11 PMID: 9482737
  5. Essential role of the small GTPase Rac in disease resistance of rice.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):759-64 PMID: 11149940
  6. Soybean GH3 promoter contains multiple auxin-inducible elements.
    Plant Cell. 1994 May;6(5):645-57 PMID: 8038604
  7. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance.
    Science. 2002 Jun 14;296(5575):2026-8 PMID: 12065837
  8. Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast.
    Plant Physiol. 1998 Oct;118(2):407-17 PMID: 9765526
  9. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis.
    Plant Cell. 2002 Apr;14(4):777-94 PMID: 11971134
  10. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking.
    Nature. 2001 Sep 27;413(6854):425-8 PMID: 11574889
  11. Rho GTPases.
    J Biol Chem. 1998 Aug 14;273(33):20685-8 PMID: 9694808
  12. Effectors for the Rho GTPases.
    Curr Opin Cell Biol. 1999 Feb;11(1):95-102 PMID: 10047515
  13. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana.
    Plant Mol Biol. 1997 Nov;35(4):483-95 PMID: 9349271
  14. Molecular analysis of an aurea photosynthetic mutant (Su/Su) in tobacco: LHCP depletion leads to pleiotropic mutant phenotypes.
    EMBO J. 1990 Dec;9(12):4197-203 PMID: 2249672
  15. Rapid induction of specific mRNAs by auxin in pea epicotyl tissue.
    J Mol Biol. 1985 May 5;183(1):53-68 PMID: 4009721
  16. Function of the ubiquitin-proteosome pathway in auxin response.
    Trends Plant Sci. 1999 Mar;4(3):107-112 PMID: 10322542
  17. Suppression of auxin signal transduction by a MAPK cascade in higher plants.
    Nature. 1998 Oct 15;395(6703):716-20 PMID: 9790195
  18. Arabidopsis RopGAPs are a novel family of rho GTPase-activating proteins that require the Cdc42/Rac-interactive binding motif for rop-specific GTPase stimulation.
    Plant Physiol. 2000 Dec;124(4):1625-36 PMID: 11115880
  19. Rho GTPases and signaling networks.
    Genes Dev. 1997 Sep 15;11(18):2295-322 PMID: 9308960
  20. Characterization of two cDNAs that encode MAP kinase homologues in Arabidopsis thaliana and analysis of the possible role of auxin in activating such kinase activities in cultured cells.
    Plant J. 1994 Jan;5(1):111-22 PMID: 8130795
  21. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles.
    Science. 2000 Feb 4;287(5454):873-80 PMID: 10657304
  22. Auxin and ethylene promote root hair elongation in Arabidopsis.
    Plant J. 1998 Dec;16(5):553-60 PMID: 10036773
  23. Genetic structure and evolution of RAC-GTPases in Arabidopsis thaliana.
    Genetics. 2000 Dec;156(4):1959-71 PMID: 11102387
  24. The Rop GTPase switch controls multiple developmental processes in Arabidopsis.
    Plant Physiol. 2001 Jun;126(2):670-84 PMID: 11402196
  25. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth.
    J Cell Biol. 1999 Apr 19;145(2):317-30 PMID: 10209027
  26. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers
    Plant Physiol. 1999 Mar;119(3):849-58 PMID: 10069824
  27. Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis.
    Plant Mol Biol. 2000 Feb;42(3):515-30 PMID: 10798620
  28. From hormone signal, via the cytoskeleton, to cell growth in single cells of tobacco.
    Cell Biol Int. 2000;24(6):343-9 PMID: 10860569
  29. AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin.
    Plant Cell. 2001 Dec;13(12):2809-22 PMID: 11752389
  30. Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean.
    Plant Cell. 1989 Feb;1(2):229-39 PMID: 2485235
  31. Activation and repression of transcription by auxin-response factors.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5844-9 PMID: 10318972
  32. Engineered GFP as a vital reporter in plants.
    Curr Biol. 1996 Mar 1;6(3):325-30 PMID: 8805250
  33. ARF1, a transcription factor that binds to auxin response elements.
    Science. 1997 Jun 20;276(5320):1865-8 PMID: 9188533
  34. How does auxin turn on genes?
    Plant Physiol. 1998 Oct;118(2):341-7 PMID: 9765520
  35. Understanding Ras: 'it ain't over 'til it's over'.
    Trends Cell Biol. 2000 Apr;10(4):147-54 PMID: 10740269
  36. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein.
    Plant Cell. 1999 Mar;11(3):393-406 PMID: 10072399
  37. The small GTP-binding protein rac is a regulator of cell death in plants.
    Proc Natl Acad Sci U S A. 1999 Sep 14;96(19):10922-6 PMID: 10485927
  38. GAPs for rho-related GTPases.
    Trends Genet. 1994 Dec;10(12):436-40 PMID: 7871593
  39. Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana.
    Genes Dev. 1999 Jul 1;13(13):1678-91 PMID: 10398681
  40. The GTPase superfamily: conserved structure and molecular mechanism.
    Nature. 1991 Jan 10;349(6305):117-27 PMID: 1898771
  41. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth.
    Plant Cell. 2002 Apr;14(4):763-76 PMID: 11971133
  42. Plant cell growth and differentiation may involve GAP regulation of Rac activity.
    FEBS Lett. 1999 Jun 25;453(3):341-5 PMID: 10405172
  43. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2940-5 PMID: 10717008
  44. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development.
    Genes Dev. 2000 Dec 1;14(23):3024-36 PMID: 11114891
  45. A Mutation Altering Auxin Homeostasis and Plant Morphology in Arabidopsis.
    Plant Cell. 1995 Dec;7(12):2023-2037 PMID: 12242367
  46. Vascular continuity and auxin signals.
    Trends Plant Sci. 2000 Sep;5(9):387-93 PMID: 10973094
  47. The Rho small G protein family-Rho GDI system as a temporal and spatial determinant for cytoskeletal control.
    Biochem Biophys Res Commun. 1998 Apr 28;245(3):641-5 PMID: 9588168
  48. Heterotrimeric and unconventional GTP binding proteins in plant cell signaling.
    Plant Cell. 2002;14 Suppl:S355-73 PMID: 12045288
  49. The auxin response of actin is altered in the rice mutant Yin-Yang.
    Protoplasma. 1998;204(1-2):22-33 PMID: 11542662
  50. Interactions and intersections of plant signaling pathways.
    J Mol Biol. 1999 Oct 22;293(2):219-34 PMID: 10550205
  51. A novel role for RhoGDI as an inhibitor of GAP proteins.
    EMBO J. 1993 May;12(5):1915-21 PMID: 8491184
  52. The ARF family of transcription factors and their role in plant hormone-responsive transcription.
    Cell Mol Life Sci. 1998 Jul;54(7):619-27 PMID: 9711229
  53. Ras and Rho GTPases: a family reunion.
    Cell. 2000 Oct 13;103(2):227-38 PMID: 11057896
  54. Degradation of Aux/IAA proteins is essential for normal auxin signalling.
    Plant J. 2000 Mar;21(6):553-62 PMID: 10758506
  55. Determination of GTP loading on Rho.
    Methods Enzymol. 2000;325:264-72 PMID: 11036609
  56. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure.
    Genes Dev. 2001 Jul 15;15(14):1808-16 PMID: 11459830
  57. Auxin-induced developmental patterns in Brassica juncea embryos.
    Development. 1998 Mar;125(5):879-87 PMID: 9449670
  58. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases.
    J Biol Chem. 1999 May 7;274(19):13198-204 PMID: 10224076
  59. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  60. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
    Plant Cell. 1997 Nov;9(11):1963-71 PMID: 9401121
  61. Auxin signaling: derepression through regulated proteolysis.
    Dev Cell. 2001 Nov;1(5):595-604 PMID: 11709180
  62. Rapid induction of selective transcription by auxins.
    Mol Cell Biol. 1985 Jun;5(6):1197-203 PMID: 4041007
  63. Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs.
    Plant Cell. 1991 Apr;3(4):419-30 PMID: 1840920
  64. Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction.
    Plant Cell. 1995 Sep;7(9):1405-19 PMID: 8589625
  65. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.
    Science. 1998 Dec 18;282(5397):2226-30 PMID: 9856939
  66. G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity.
    Cell Signal. 2002 May;14(5):397-405 PMID: 11882384
  67. Site-directed mutagenesis by overlap extension using the polymerase chain reaction.
    Gene. 1989 Apr 15;77(1):51-9 PMID: 2744487
  68. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis.
    Science. 2001 Jun 15;292(5524):2066-9 PMID: 11408654
  69. Small GTPases: versatile signaling switches in plants.
    Plant Cell. 2002;14 Suppl:S375-88 PMID: 12045289
  70. Transient expression analysis in plants using firefly luciferase reporter gene.
    Methods Enzymol. 1992;216:397-414 PMID: 1479911
  71. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth.
    EMBO J. 2001 Jun 1;20(11):2779-88 PMID: 11387211
  72. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF.
    Science. 1999 Oct 8;286(5438):316-8 PMID: 10514379
  73. Plant GTPases: the Rhos in bloom.
    Trends Cell Biol. 2000 Apr;10(4):141-6 PMID: 10740268
  74. One plant actin isovariant, ACT7, is induced by auxin and required for normal callus formation.
    Plant Cell. 2001 Jul;13(7):1541-54 PMID: 11449050
  75. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana.
    Genes Dev. 1998 Jul 15;12(14):2175-87 PMID: 9679062
  76. A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction.
    Gene. 1991 Jun 15;102(1):67-70 PMID: 1864511
  77. Early genes and auxin action.
    Plant Physiol. 1996 May;111(1):9-17 PMID: 8685277
  78. EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7.
    Cell. 1994 Jul 1;77(7):1051-62 PMID: 8020095
  79. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization.
    Planta. 1996;200(2):229-37 PMID: 8904808
  80. Conservation and innovation in plant signaling pathways.
    Cell. 2000 Oct 13;103(2):201-9 PMID: 11057894
  81. Inactivation of auxin in tobacco transformed with the indoleacetic acid-lysine synthetase gene of Pseudomonas savastanoi.
    Genes Dev. 1991 Mar;5(3):438-46 PMID: 2001843
  82. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4985-90 PMID: 10781109
  83. G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells.
    Science. 2001 Jun 15;292(5524):2070-2 PMID: 11408655
  84. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes.
    J Cell Biol. 2001 Mar 5;152(5):1019-32 PMID: 11238457
  85. Roles and activities of Aux/IAA proteins in Arabidopsis.
    Trends Plant Sci. 2001 Sep;6(9):420-5 PMID: 11544131
  86. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana.
    J Mol Biol. 1995 Aug 25;251(4):533-49 PMID: 7658471
  87. Redundancy as a way of life - IAA metabolism.
    Curr Opin Plant Biol. 1999 Jun;2(3):207-13 PMID: 10375566
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.006320
Published
2002-11-00
Pages
2745-60
Language
English
Region
England
NLM ID
9208688
PMCID
PMC152724
Subset
IM
Databases
GENBANK
AY029330
External Links
PubMed source DOI: 10.1105/tpc.006320 PMC Full Text View journal details
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