Home LiteratureArticle Details
PMID: 11387211 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth.

The EMBO journal ·Vol. 20 ·No. 11 ·2001-06-01 ·Pages 2779-88

Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K

Abstract

Plants contain a novel unique subfamily of Rho GTPases, vital components of cellular signalling networks. Here we report a general role for some members of this family in polarized plant growth processes. We show that Arabidopsis AtRop4 and AtRop6 encode functional GTPases with similar intrinsic GTP hydrolysis rates. We localized AtRop proteins in root meristem cells to the cross-wall and cell plate membranes. Polar localization of AtRops in trichoblasts specifies the growth sites for emerging root hairs. These sites were visible before budding and elongation of the Arabidopsis root hair when AtRops accumulated at their tips. Expression of constitutively active AtRop4 and AtRop6 mutant proteins in root hairs of transgenic Arabidopsis plants abolished polarized growth and delocalized the tip-focused Ca2+ gradient. Polar localization of AtRops was inhibited by brefeldin A, but not by other drugs such as latrunculin B, cytochalasin D or caffeine. Our results demonstrate a general function of AtRop GTPases in tip growth and in polar diffuse growth.

Keywords
Non-programmatic
MeSH Terms
Arabidopsis/cytology,enzymology,growth & development Calcium/metabolism Cell Line Cytoskeleton/enzymology,ultrastructure GTP Phosphohydrolases/genetics,metabolism Immunohistochemistry Microtubules/enzymology,ultrastructure Plant Proteins/metabolism Plant Roots/cytology,enzymology,growth & development Plants, Toxic Recombinant Proteins/metabolism Tobacco Transfection
Chemicals
Plant Proteins Recombinant Proteins GTP Phosphohydrolases Calcium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Molendijk A J
Max-Delbrück-Laboratorium in der Max-Planck-Gesellschaft and Max-Planck Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, D-50829 Köln, Germany.
Bischoff F
Rajendrakumar C S
Friml J
Braun M
Gilroy S
Palme K
References (52)
52 references, click to expand
  1. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase.
    Gene. 1988 Jul 15;67(1):31-40 PMID: 3047011
  2. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity.
    Mol Biol Cell. 1993 Dec;4(12):1307-16 PMID: 8167411
  3. Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs
    Planta. 1999 Oct;209(4):435-43 PMID: 10550624
  4. Role of Dictyostelium racE in cytokinesis: mutational analysis and localization studies by use of green fluorescent protein.
    Mol Biol Cell. 1997 May;8(5):935-44 PMID: 9168476
  5. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana.
    Plant J. 1997 Aug;12(2):427-39 PMID: 9301093
  6. Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5888-93 PMID: 8650188
  7. Signaling to Rho GTPases.
    Exp Cell Res. 1999 Nov 25;253(1):166-79 PMID: 10579921
  8. Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges.
    Dev Biol. 2000 Nov 15;227(2):618-32 PMID: 11071779
  9. Constructing a plant cell. The genetic control of root hair development.
    Plant Physiol. 2000 Dec;124(4):1525-31 PMID: 11115870
  10. 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
  11. AtPIN2 defines a locus of Arabidopsis for root gravitropism control.
    EMBO J. 1998 Dec 1;17(23):6903-11 PMID: 9843496
  12. The Rrop GTPase switch turns on polar growth in pollen.
    Trends Plant Sci. 2000 Jul;5(7):298-303 PMID: 10871902
  13. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana.
    Plant Mol Biol. 1997 Nov;35(4):483-95 PMID: 9349271
  14. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae.
    J Cell Biol. 1994 Jun;125(5):1077-93 PMID: 8195291
  15. Tip-localized calcium entry fluctuates during pollen tube growth.
    Dev Biol. 1996 Feb 25;174(1):160-73 PMID: 8626016
  16. Rho GTPases and signaling networks.
    Genes Dev. 1997 Sep 15;11(18):2295-322 PMID: 9308960
  17. Measurement of intrinsic nucleotide exchange and GTP hydrolysis rates.
    Methods Enzymol. 1995;256:67-76 PMID: 7476456
  18. Cytoskeletal control of polar growth in plant cells.
    Curr Opin Cell Biol. 1998 Feb;10(1):117-22 PMID: 9484603
  19. 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
  20. Digging out roots: pattern formation, cell division, and morphogenesis in plants.
    Curr Top Dev Biol. 1999;45:207-47 PMID: 10332606
  21. 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
  22. The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process.
    Plant Physiol. 1994 Dec;106(4):1335-1346 PMID: 12232412
  23. Genes encoding small GTP-binding proteins analogous to mammalian rac are preferentially expressed in developing cotton fibers.
    Mol Gen Genet. 1995 Jul 22;248(1):43-51 PMID: 7651326
  24. GTP-binding proteins in plants.
    Cell Mol Life Sci. 1999 Feb;55(2):233-56 PMID: 10188584
  25. Sequence dependence of protein isoprenylation.
    J Biol Chem. 1991 Aug 5;266(22):14603-10 PMID: 1860864
  26. A glucocorticoid-inducible transcription system causes severe growth defects in Arabidopsis and induces defense-related genes.
    Plant J. 1999 Oct;20(1):127-33 PMID: 10571872
  27. Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth.
    Plant Cell. 1997 Sep;9(9):1647-1659 PMID: 12237397
  28. Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall.
    Plant J. 1999 Sep;19(5):555-67 PMID: 10504577
  29. Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling.
    Cell Signal. 1999 Aug;11(8):545-54 PMID: 10433515
  30. 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
  31. Transgenic tobacco plants that express an antisense construct derived from a Medicago sativa cDNA encoding a Rac-related small GTP-binding protein fail to develop necrotic lesions upon elicitor infiltration.
    Mol Gen Genet. 2000 Jun;263(5):761-70 PMID: 10905344
  32. 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
  33. Signaling tip growth in plants.
    Curr Opin Plant Biol. 1998 Dec;1(6):525-30 PMID: 10066628
  34. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx.
    Plant Cell. 1999 Sep;11(9):1731-42 PMID: 10488239
  35. Rho GTPases and the actin cytoskeleton.
    Science. 1998 Jan 23;279(5350):509-14 PMID: 9438836
  36. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein.
    J Biol Chem. 1997 Sep 12;272(37):23371-5 PMID: 9287351
  37. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):54-105 PMID: 10066831
  38. A glucocorticoid-mediated transcriptional induction system in transgenic plants.
    Plant J. 1997 Mar;11(3):605-12 PMID: 9107046
  39. Molecular cloning and characterization of rho, a ras-related small GTP-binding protein from the garden pea.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8732-6 PMID: 8378356
  40. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding.
    J Cell Biol. 2001 Jan 8;152(1):111-26 PMID: 11149925
  41. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  42. The growing cell plate of higher plants is a site of both actin assembly and vinculin-like antigen recruitment.
    Eur J Cell Biol. 1998 Sep;77(1):10-8 PMID: 9808284
  43. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones.
    Plant Physiol. 1994 Dec;106(4):1241-55 PMID: 7846151
  44. Signaling to the actin cytoskeleton.
    Annu Rev Cell Dev Biol. 1998;14:305-38 PMID: 9891786
  45. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.
    Science. 1998 Dec 18;282(5397):2226-30 PMID: 9856939
  46. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae.
    EMBO J. 1997 May 15;16(10):2745-55 PMID: 9184220
  47. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF.
    Science. 1999 Oct 8;286(5438):316-8 PMID: 10514379
  48. CYTOSKELETAL PERSPECTIVES ON ROOT GROWTH AND MORPHOGENESIS.
    Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:289-322 PMID: 15012194
  49. Plant GTPases: the Rhos in bloom.
    Trends Cell Biol. 2000 Apr;10(4):141-6 PMID: 10740268
  50. Localization of a Rho GTPase Implies a Role in Tip Growth and Movement of the Generative Cell in Pollen Tubes.
    Plant Cell. 1996 Feb;8(2):293-303 PMID: 12239385
  51. Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana.
    Plant J. 1999 Mar;17(6):657-65 PMID: 10230063
  52. Cell morphogenesis in Arabidopsis.
    Bioessays. 1998 Jan;20(1):20-9 PMID: 9504044
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2001-06-01
Pages
2779-88
Language
English
Region
England
NLM ID
8208664
PMCID
PMC125484
Subset
IM
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