Skip to main content
SpringerLink
Log in

Regulatory and Cellular Functions of Plant RhoGAPs and RhoGDIs

  • Chapter
  • First Online:
Integrated G Proteins Signaling in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Rho GTPases play central roles in the regulation of essential cellular processes, such as directional expansion, motility, and division. RhoGEFs (Guanine Nucleotide Exchange Factors) have key functions in the stimulus-induced spatio-temporal control of Rho GTPase activity. RhoGAPs (GTPase activating proteins) and RhoGDIs (Guanine nucleotide dissociation inhibitors) have long been seen as less important regulators of Rho GTPase activity, with functions largely restricted to the constitutive attenuation of Rho signaling. Extended families of diverse RhoGAPs, as well as small families of structurally similar RhoGDIs, have been identified in yeast, animals, and plants. Recent research has established that members of these protein families play much more important and complex roles than previously anticipated in the regulation of Rho GTPase activity and cellular processes. Non-plant RhoGAPs and RhoGDIs were shown to be tightly regulated by upstream signaling, and the same is likely to be true for their plant homologs as well. The recent functional characterization of plant RhoGAPs and RhoGDIs has allowed exciting and universally important insights into the molecular mechanisms underlying the control of Rho GTPase activity by these proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aitken A (2002) Functional specificity in 14–3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants. Plant Mol Biol 50:993–1010

    Article  CAS  PubMed  Google Scholar 

  • Anderson DC, Gill JS, Cinalli RM, Nance J (2008) Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts. Science 320:1771–1774

    Article  CAS  PubMed  Google Scholar 

  • Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) ROPGAP4-dependent ROP GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028

    Article  CAS  PubMed  Google Scholar 

  • Berken A, Thomas C, Wittinghofer A (2005) A new family of RhoGEFs activates the ROP molecular switch in plants. Nature 436:1176–1180

    Article  CAS  PubMed  Google Scholar 

  • Bernards A (2003) GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim Biophys Acta 1603:47–82

    CAS  PubMed  Google Scholar 

  • Bernards A, Settleman J (2004) GAP control: regulating the regulators of small GTPases. Trends Cell Biol 14:377–385

    Article  CAS  PubMed  Google Scholar 

  • Bokoch GM (1994) Regulation of the human neutrophil NADPH oxidase by the Rac GTP-binding proteins. Curr Opin Cell Biol 6:212–218

    Article  CAS  PubMed  Google Scholar 

  • Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016

    Article  CAS  PubMed  Google Scholar 

  • Chiang SH, Hwang J, Legendre M, Zhang M, Kimura A, Saltiel AR (2003) TCGAP, a multidomain Rho GTPase-activating protein involved in insulin-stimulated glucose transport. EMBO J 22:2679–2691

    Article  CAS  PubMed  Google Scholar 

  • Christensen HEM, Ramachandran S, Tan C-T, Surana U, Dong C-H, Chua N-H (1996) Arabidopsis profilins are functionally similar to yeast profilins: identification of a vascular bundle-specific profilin and a pollen-specific profilin. Plant J 10:269–279

    Article  CAS  PubMed  Google Scholar 

  • Chuang TH, Bohl BP, Bokoch GM (1993) Biologically active lipids are regulators of Rac.GDI complexation. J Biol Chem 268:26206–26211

    CAS  PubMed  Google Scholar 

  • Del Pozo MA, Kiosses WB, Alderson NB, Meller N, Hahn KM, Schwartz MA (2002) Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat Cell Biol 4:232–239

    Article  PubMed  Google Scholar 

  • DerMardirossian C, Bokoch GM (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 15:356–363

    Article  CAS  PubMed  Google Scholar 

  • DerMardirossian C, Rocklin G, Seo JY, Bokoch GM (2006) Phosphorylation of RhoGDI by Src regulates Rho GTPase binding and cytosol-membrane cycling. Mol Biol Cell 17:4760–4768

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–635

    Article  CAS  PubMed  Google Scholar 

  • Fauré J, Vignais PV, Dagher MC (1999) Phosphoinositide-dependent activation of Rho A involves partial opening of the RhoA/Rho-GDI complex. Eur J Biochem 262:879–889

    Article  PubMed  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Fritz G, Lang P, Just I (1994) Tissue-specific variations in the expression and regulation of the small GTP-binding protein Rho. Biochim Biophys Acta 1222:331–338

    Article  CAS  PubMed  Google Scholar 

  • Graham DL, Eccleston JF, Lowe PN (1999) The conserved arginine in rho-GTPase-activating protein is essential for efficient catalysis but not for complex formation with Rho.GDP and aluminum fluoride. Biochemistry 38:985–991

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Li S, Lord EM, Yang Z (2006) Members of a novel class of Arabidopsis Rho Guanine Nucleotide Exchange Factors control Rho GTPase-dependent polar growth. Plant Cell 18:366–381

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Wang Z, Yang Z (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Opin Plant Biol 7:527–536

    Article  CAS  PubMed  Google Scholar 

  • Helling D, Possart A, Cottier S, Klahre U, Kost B (2006) Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18:3519–3534

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    Article  CAS  PubMed  Google Scholar 

  • Hoffman GR, Nassar N, Cerione RA (2000) Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100:345–356

    Article  CAS  PubMed  Google Scholar 

  • Hwang J-U, Vernoud V, Szumlanski A, Nielsen E, Yang Z (2008) A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr Biol 18:1907–1916

    Article  CAS  PubMed  Google Scholar 

  • Hwang JU, Gu Y, Lee YJ, Yang Z (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16:5385–5399

    Article  CAS  PubMed  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    Article  CAS  PubMed  Google Scholar 

  • Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis ROP2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763–776

    Article  CAS  PubMed  Google Scholar 

  • Klahre U, Becker C, Schmitt AC, Kost B (2006) Nt-RhoGDI2 regulates Rac/ROP signaling and polar cell growth in tobacco pollen tubes. Plant J 46:1018–1031

    Article  CAS  PubMed  Google Scholar 

  • Klahre U, Kost B (2006) Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/ROP to the apex of pollen tubes. Plant Cell 18:3033–3046

    Article  CAS  PubMed  Google Scholar 

  • Knaus M, Pelli-Gulli MP, van Drogen F, Springer S, Jaquenoud M, Peter M (2007) Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J 26:4501–4513

    Article  CAS  PubMed  Google Scholar 

  • Knezevic N, Roy A, Timblin B, Konstantoulaki M, Sharma T, Malik AB, Mehta D (2007) GDI-1 phosphorylation switch at serine 96 induces RhoA activation and increased endothelial permeability. Mol Cell Biol 27:6323–6333

    Article  CAS  PubMed  Google Scholar 

  • Kost B (2008) Spatial control of Rho (Rac-ROP) signaling in tip-growing plant cells. Trends Cell Biol 18:119–127

    Article  CAS  PubMed  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    Article  CAS  PubMed  Google Scholar 

  • Lamarche N, Hall A (1994) GAPs for rho-related GTPases. Trends Genet 10:436–440

    Article  CAS  PubMed  Google Scholar 

  • Li H, Lin YK, Heath RM, Zhu MX, Yang ZB (1999) Control of pollen tube tip growth by a ROP GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1742

    Article  CAS  PubMed  Google Scholar 

  • Lin Q, Fuji RN, Yang W, Cerione RA (2003) RhoGDI is required for Cdc42-mediated cellular transformation. Curr Biol 13:1469–1479

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Wang Y, Zhu J-K, Yang Z (1996) Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8:293–303

    Article  CAS  PubMed  Google Scholar 

  • Masuda T, Tanaka K, Nonaka H, Yamochi W, Maeda A, Takai Y (1994) Molecular cloning and characterization of yeast rho GDP dissociation inhibitor. J Biol Chem 269:19713–19718

    CAS  PubMed  Google Scholar 

  • Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, Philips MR (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152:111–126

    Article  CAS  PubMed  Google Scholar 

  • Molendijk AJ, Bischoff F, Rajendrakumar CSV, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana ROP GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–2788

    Article  CAS  PubMed  Google Scholar 

  • Nebenführ A, Ritzenthaler C, Robinson DG (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol 130:1102–1108

    Article  PubMed  Google Scholar 

  • Nibau C, Wu HM, Cheung AY (2006) RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trends Plant Sci 11:309–315

    Article  CAS  PubMed  Google Scholar 

  • Nomanbhoy TK, Cerione RA (1996) Characterization of the interaction between RhoGDI and Cdc42Hs using fluorescence spectroscopy. J Biol Chem 271:10004–10009

    Article  CAS  PubMed  Google Scholar 

  • Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98:759–764

    Article  CAS  PubMed  Google Scholar 

  • Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    CAS  PubMed  Google Scholar 

  • Pirone DM, Carter DE, Burbelo PD (2001) Evolutionary expansion of CRIB-containing Cdc42 effector proteins. Trends Genet 17:370–373

    Article  CAS  PubMed  Google Scholar 

  • Potocky M, Jones MA, Bezvoda R, Smirnoff N, Zarsky V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    Article  CAS  PubMed  Google Scholar 

  • Qiao J, Holian O, Lee BS, Huang F, Zhang J, Lum H (2008) Phosphorylation of GTP dissociation inhibitor by PKA negatively regulates RhoA. Am J Physiol Cell Physiol 295:C1161–1168

    Article  CAS  PubMed  Google Scholar 

  • Read SM, Clarke AE, Bacic A (1993) Stimulation of growth of cultured Nicotiana tabacum W38 pollen tubes by poly(ethylene glycol) and Cu(II) salts. Protoplasma 177:1–14

    Article  CAS  Google Scholar 

  • Ren XR, Du QS, Huang YZ, Ao SZ, Mei L, Xiong WC (2001) Regulation of CDC42 GTPase by proline-rich tyrosine kinase 2 interacting with PSGAP, a novel pleckstrin homology and Src homology 3 domain containing rhoGAP protein. J Cell Biol 152:971–984

    Article  CAS  PubMed  Google Scholar 

  • Rittinger K, Walker PA, Eccleston JF, Smerdon SJ, Gamblin SJ (1997) Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389:758–762

    Article  CAS  PubMed  Google Scholar 

  • Rossman KL, Der CJ, Sondek J (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6:167–180

    Article  CAS  PubMed  Google Scholar 

  • Scheffzek K, Stephan I, Jensen ON, Illenberger D, Gierschik P (2000) The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nat Struct Biol 7:122–126

    Article  CAS  PubMed  Google Scholar 

  • Scholz RP, Regner J, Theil A, Erlmann P, Holeiter G, Jahne R, Schmid S, Hausser A, Olayioye MA (2009) DLC1 interacts with 14–3-3 proteins to inhibit RhoGAP activity and block nucleocytoplasmic shuttling. J Cell Sci 122:92–102

    Article  CAS  PubMed  Google Scholar 

  • Simoes S, Denholm B, Azevedo D, Sotillos S, Martin P, Skaer H, Hombria JC, Jacinto A (2006) Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133:4257–4267

    Article  CAS  PubMed  Google Scholar 

  • Strassheim D, Porter RA, Phelps SH, Williams CL (2000) Unique in vivo associations with SmgGDS and RhoGDI and different Guanine Nucleotide Exchange activities exhibited by RhoA, dominant negative RhoAAsn-19, and activated RhoAVal-14. J Biol Chem 275:6699–6702

    Article  CAS  PubMed  Google Scholar 

  • Szumlanski AL, Nielsen E (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21:526–544

    Article  CAS  PubMed  Google Scholar 

  • Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244

    Article  CAS  PubMed  Google Scholar 

  • Tcherkezian J, Lamarche-Vane N (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99:67–86

    Article  CAS  PubMed  Google Scholar 

  • Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev 5:496–507

    Article  CAS  PubMed  Google Scholar 

  • Ueda T, Kikuchi A, Ohga N, Yamamoto J, Takai Y (1990) Purification and characterization from bovine brain cytosol of a novel regulatory protein inhibiting the dissociation of GDP from and the subsequent binding of GTP to rhoB p20, a ras p21-like GTP-binding protein. J Biol Chem 265:9373–9380

    CAS  PubMed  Google Scholar 

  • Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208

    Article  CAS  PubMed  Google Scholar 

  • Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12:2534–2545

    CAS  PubMed  Google Scholar 

  • Wennerberg K, Der CJ (2004) Rho-family GTPases: it's not only Rac and Rho (and I like it). J Cell Sci 117:1301–1312

    Article  CAS  PubMed  Google Scholar 

  • Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:581–590

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Li H, Yang ZB (2000) 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 124:1625–1636

    Article  CAS  PubMed  Google Scholar 

  • Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol 147:1527–1543

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Pellman D (2008) Plugging the GAP between cell polarity and cell cycle. EMBO Rep 9:39–41

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

BK thanks DFG, BBSRC, VR, and FORMAS for funding.

Author information

Authors and Affiliations

  1. Uppsala BioCenter, Plant Biology and Forest Genetics, Swedish University of Agricultural Sciences, 7080, 75007, Uppsala, Sweden

    Benedikt Kost

Authors
  1. Benedikt Kost
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benedikt Kost .

Editor information

Editors and Affiliations

  1. Dept. Plant Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv, 69978, Israel

    Shaul Yalovsky

  2. Inst. Zelluläre und Molekulare, Universität Bonn, Kirschallee 1, Bonn, 53115, Germany

    František Baluška

  3. Dept. Biology & Pharmacology, University of North Carolina, Coker Hall 317, Chapel Hill, 27599, U.S.A.

    Alan Jones

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kost, B. (2010). Regulatory and Cellular Functions of Plant RhoGAPs and RhoGDIs. In: Yalovsky, S., Baluška, F., Jones, A. (eds) Integrated G Proteins Signaling in Plants. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-03524-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation