ROP GTPases and Cell Shape

  • Daria Bloch
  • Gil Feiguelman
  • Ella Buriakovsky
  • Shaul Yalovsky
Living reference work entry


Plants produce multiple forms of the Rho-like GTPases in the Ras superfamily that are evolutionarily distinct from their animal and fungal counterparts.


Pollen Tube Root Hair Cortical Microtubule Pavement Cell Tobacco Pollen Tube 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The preparation of this chapter was enabled by the support from the Israel Science Foundation (ISF 1244/11), the Israeli Centers for Research Excellence (I-CORE 757/12), the ISF-NCSF (ISF-China 1125/13), and the German Research Foundation’s Germany–Palestinian Authority–Israel Trilateral Program (DFG KU 931/13-1) to SY.


  1. Basu D, El-Assal Sel D, Le J, Mallery EL, Szymanski DB. Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development. 2004;131(17):4345–55.PubMedGoogle Scholar
  2. Basu D, Le J, El-Essal Sel D, Huang S, Zhang C, Mallery EL, Koliantz G, Staiger CJ, Szymanski DB. DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell. 2005;17(2):502–24.PubMedCentralPubMedGoogle Scholar
  3. Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB. A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci U S A. 2008;105(10):4044–9.PubMedCentralPubMedGoogle Scholar
  4. Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science. 2002;296(5575):2026–8.PubMedGoogle Scholar
  5. Berken A, Wittinghofer A. Structure and function of Rho-type molecular switches in plants. Plant Physiol Biochem. 2008;46(3):380–93.PubMedGoogle Scholar
  6. Berken A, Thomas C, Wittinghofer A. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature. 2005;436(7054):1176–80.PubMedGoogle Scholar
  7. Bischoff F, Vahlkamp L, Molendijk A, Palme K. Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Mol Biol. 2000;42(3):515–30.PubMedGoogle Scholar
  8. Bloch D, Yalovsky S. Cell polarity signaling. Curr Opin Plant Biol. 2013;16(6):734–42.PubMedGoogle Scholar
  9. Bloch D, Lavy M, Efrat Y, Efroni I, Bracha-Drori K, Abu-Abied M, Sadot E, Yalovsky S. Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol Biol Cell. 2005;16(4):1913–27.PubMedCentralPubMedGoogle Scholar
  10. Bloch D, Monshausen G, Singer M, Gilroy S, Yalovsky S. Nitrogen source interacts with ROP signalling in root hair tip-growth. Plant Cell Environ. 2011;34(1):76–88.PubMedGoogle Scholar
  11. Borg S, Podenphant L, Jensen TJ, Poulsen C. Plant cell growth and differentiation may involve GAP regulation of Rac activity. FEBS Lett. 1999;453(3):341–345PubMedGoogle Scholar
  12. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol. 2010;12(5):477–83.PubMedCentralPubMedGoogle Scholar
  13. Boureux A, Vignal E, Faure S, Fort P. Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol. 2007;24(1):203–16.PubMedCentralPubMedGoogle Scholar
  14. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991;349(6305):117–27.PubMedGoogle Scholar
  15. Brembu T, Winge P, Bones AM, Yang Z. A RHOse by any other name: a comparative analysis of animal and plant Rho GTPases. Cell Res. 2006;16(5):435–45.PubMedGoogle Scholar
  16. Burbelo PD, Drechsel D, Hall A. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem. 1995;270(49):29071–4.PubMedGoogle Scholar
  17. Caldelari D, Sternberg H, Rodriguez-Concepcion M, Gruissem W, Yalovsky S. Efficient prenylation by a plant geranylgeranyltransferase-I requires a functional CaaL box motif and a proximal polybasic domain. Plant Physiol. 2001;126(4):1416–29.PubMedCentralPubMedGoogle Scholar
  18. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature. 2005;438(7070):1013–6.PubMedGoogle Scholar
  19. Chang F, Gu Y, Ma H, Yang Z. AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth. Mol Plant. 2013;6(4):1187–201.PubMedCentralPubMedGoogle Scholar
  20. Chen CY, Cheung AY, Wu HM. Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell. 2003;15(1):237–49.PubMedCentralPubMedGoogle Scholar
  21. Chen M, Liu H, Kong J, Yang Y, Zhang N, Li R, Yue J, Huang J, Li C, Cheung AY, Tao LZ. RopGEF7 regulates PLETHORA-dependent maintenance of the root stem cell niche in Arabidopsis. Plant Cell. 2011;23(8):2880–94.PubMedCentralPubMedGoogle Scholar
  22. Chen X, Naramoto S, Robert S, Tejos R, Lofke C, Lin D, Yang Z, Friml J. ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr Biol. 2012;22(14):1326–32.PubMedGoogle Scholar
  23. Christensen TM, Vejlupkova Z, Sharma YK, Arthur KM, Spatafora JW, Albright CA, Meeley RB, Duvick JP, Quatrano RS, Fowler JE. Conserved subgroups and developmental regulation in the monocot rop gene family. Plant Physiol. 2003;133(4):1791–808.PubMedCentralPubMedGoogle Scholar
  24. Cole RA, Synek L, Zarsky V, Fowler JE. SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 2005;138(4):2005–18.PubMedCentralPubMedGoogle Scholar
  25. Colicelli J. Human RAS superfamily proteins and related GTPases. Sci STKE. 2004;2004(250):RE13.PubMedCentralPubMedGoogle Scholar
  26. DerMardirossian C, Schnelzer A, Bokoch GM. Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol Cell. 2004;15(1):117–27.PubMedGoogle Scholar
  27. Duan Q, Kita D, Li C, Cheung AY, Wu HM. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci U S A. 2010;107(41):17821–6.PubMedCentralPubMedGoogle Scholar
  28. Dvorsky R, Ahmadian MR. Always look on the bright site of Rho: structural implications for a conserved intermolecular interface. EMBO Rep. 2004;5(12):1130–6.PubMedCentralPubMedGoogle Scholar
  29. Eklund DM, Svensson EM, Kost B. Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth. J Exp Bot. 2010;61(7):1917–37.PubMedGoogle Scholar
  30. Elias M. The guanine nucleotide exchange factors Sec2 and PRONE: candidate synapomorphies for the Opisthokonta and the Archaeplastida. Mol Biol Evol. 2008;25(8):1526–9.PubMedGoogle Scholar
  31. Elias M, Klimes V. Rho GTPases: deciphering the evolutionary history of a complex protein family. Methods Mol Biol. 2012;827:13–34.PubMedGoogle Scholar
  32. Elias M, Drdova E, Ziak D, Bavlnka B, Hala M, Cvrckova F, Soukupova H, Zarsky V. The exocyst complex in plants. Cell Biol Int. 2003;27(3):199–201.PubMedGoogle Scholar
  33. Feig LA. Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat Cell Biol. 1999;1(2):E25–7.PubMedGoogle Scholar
  34. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422(6930):442–6.PubMedGoogle Scholar
  35. Fowler J. Evolution of the ROP GTPase signaling module. In: Yalovsky S, Baluška F, Jones A, editors. Integrated G proteins signaling in plants. Berlin/Heidelberg: Springer; 2010. p. 305–27.Google Scholar
  36. Freeman JL, Abo A, Lambeth JD. Rac “insert region” is a novel effector region that is implicated in the activation of NADPH oxidase, but not PAK65. J Biol Chem. 1996;271(33):19794–801.PubMedGoogle Scholar
  37. Fricke I, Berken A. Molecular basis for the substrate specificity of plant guanine nucleotide exchange factors for ROP. FEBS Lett. 2009;583(1):75–80.PubMedGoogle Scholar
  38. Fu Y, Wu G, Yang Z. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol. 2001;152(5):1019–32.PubMedCentralPubMedGoogle Scholar
  39. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell. 2005;120(5):687–700.PubMedGoogle Scholar
  40. Fukumoto Y, Kaibuchi K, Hori Y, Fujioka H, Araki S, Ueda T, Kikuchi A, Takai Y. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene. 1990;5(9):1321–8.PubMedGoogle Scholar
  41. Garcia-Mata R, Boulter E, Burridge K. The ‘invisible hand’: regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol. 2011;12(8):493–504.PubMedCentralPubMedGoogle Scholar
  42. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell. 2003;112(2):219–30.PubMedGoogle Scholar
  43. Grunt M, Zarsky V, Cvrckova F. Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing proteins. BMC Evol Biol. 2008;8:115.PubMedCentralPubMedGoogle Scholar
  44. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol. 2005;169(1):127–38.PubMedCentralPubMedGoogle Scholar
  45. Gu Y, Li S, Lord EM, Yang Z. Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. Plant Cell. 2006;18(2):366–81.PubMedCentralPubMedGoogle Scholar
  46. Guo W, Tamanoi F, Novick P. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat Cell Biol. 2001;3(4):353–60.PubMedGoogle Scholar
  47. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol. 2009;11(7):797–806.PubMedGoogle Scholar
  48. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell. 2008;20(5):1330–45.PubMedCentralPubMedGoogle Scholar
  49. Hall A. Rho family GTPases. Biochem Soc Trans. 2012;40(6):1378–82.PubMedGoogle Scholar
  50. Hart MJ, Maru Y, Leonard D, Witte ON, Evans T, Cerione RA. A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science. 1992;258(5083):812–5.PubMedGoogle Scholar
  51. Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S. A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 2010;8(1):e1000282.PubMedCentralPubMedGoogle Scholar
  52. Hazak O, Obolski U, Prat T, Friml J, Hadany L, Yalovsky S. Bimodal regulation of ICR1 levels generates self-organizing auxin distribution. Proc Natl Acad Sci U S A. 2014;111(50):E5471–9.PubMedCentralPubMedGoogle Scholar
  53. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science. 2006;314(5804):1458–61.PubMedCentralPubMedGoogle Scholar
  54. Hoefle C, Huckelhoven R. A barley Engulfment and Motility domain containing protein modulates Rho GTPase activating protein HvMAGAP1 function in the barley powdery mildew interaction. Plant Mol Biol. 2014;84(4–5):469–8.Google Scholar
  55. Hoefle C, Huesmann C, Schultheiss H, Bornke F, Hensel G, Kumlehn J, Huckelhoven R. A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell. 2011;23(6):2422–39.PubMedCentralPubMedGoogle Scholar
  56. Hoffman GR, Nassar N, Cerione RA. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell. 2000;100(3):345–56.PubMedGoogle Scholar
  57. Huang TY, DerMardirossian C, Bokoch GM. Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol. 2006;18(1):26–31.PubMedGoogle Scholar
  58. Huesmann C, Hoefle C, Huckelhoven R. ROPGAPs of Arabidopsis limit susceptibility to powdery mildew. Plant Signal Behav. 2011;6(11):1691–4.PubMedCentralPubMedGoogle Scholar
  59. Huesmann C, Reiner T, Hoefle C, Preuss J, Jurca ME, Domoki M, Feher A, Huckelhoven R. Barley ROP binding kinase1 is involved in microtubule organization and in basal penetration resistance to the barley powdery mildew fungus. Plant Physiol. 2012;159(1):311–20.PubMedCentralPubMedGoogle Scholar
  60. Hwang JU, Vernoud V, Szumlanski A, Nielsen E, Yang Z. A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr Biol. 2008;18(24):1907–16.PubMedCentralPubMedGoogle Scholar
  61. Hwang JU, Wu G, Yan A, Lee YJ, Grierson CS, Yang Z. Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J Cell Sci. 2010;123(Pt 3):340–50.PubMedCentralPubMedGoogle Scholar
  62. Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell. 2002;14(4):763–76.PubMedCentralPubMedGoogle Scholar
  63. Kaothien P, Ok SH, Shuai B, Wengier D, Cotter R, Kelley D, Kiriakopolos S, Muschietti J, McCormick S. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant J. 2005;42(4):492–503.PubMedGoogle Scholar
  64. Karnoub AE, Der CJ, Campbell SL. The insert region of Rac1 is essential for membrane ruffling but not cellular transformation. Mol Cell Biol. 2001;21(8):2847–57.PubMedCentralPubMedGoogle Scholar
  65. Klahre U, Kost B. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell. 2006;18(11):3033–46.PubMedCentralPubMedGoogle Scholar
  66. Klahre U, Becker C, Schmitt AC, Kost B. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J. 2006;46(6):1018–31.PubMedGoogle Scholar
  67. Kost B. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol. 2008;18(3):119–27.PubMedGoogle Scholar
  68. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol. 1999;145(2):317–30.PubMedCentralPubMedGoogle Scholar
  69. Lamarche N, Hall A. GAPs for rho-related GTPases. Trends Genet. 1994;10(12):436–40.PubMedGoogle Scholar
  70. Lavy M, Yalovsky S. Association of Arabidopsis type-II ROPs with the plasma membrane requires a conserved C-terminal sequence motif and a proximal polybasic domain. Plant J. 2006;46(6):934–47.PubMedGoogle Scholar
  71. Lavy M, Bracha-Drori K, Sternberg H, Yalovsky S. A cell-specific, prenylation-independent mechanism regulates targeting of type II RACs. Plant Cell. 2002;14(10):2431–50.PubMedCentralPubMedGoogle Scholar
  72. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S. A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol. 2007;17(11):947–52.PubMedGoogle Scholar
  73. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol. 2008;9(2):99–111.PubMedGoogle Scholar
  74. Li S, Gu Y, Yan A, Lord E, Yang ZB. RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant. 2008;1(6):1021–35.PubMedGoogle Scholar
  75. Lin D, Cao L, Zhou Z, Zhu L, Ehrhardt D, Yang Z, Fu Y. Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr Biol. 2013;23(4):290–7.PubMedGoogle Scholar
  76. Madaule P, Axel R. A novel ras-related gene family. Cell. 1985;41(1):31–40.PubMedGoogle Scholar
  77. Mathur J. Local interactions shape plant cells. Curr Opin Cell Biol. 2006;18(1):40–6.PubMedGoogle Scholar
  78. Millard TH, Sharp SJ, Machesky LM. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J. 2004;380(Pt 1):1–17.PubMedCentralPubMedGoogle Scholar
  79. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 2001;20(11):2779–88.PubMedCentralPubMedGoogle Scholar
  80. Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z. ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 2012;10(4):e1001299.PubMedCentralPubMedGoogle Scholar
  81. Obsil T, Obsilova V. Structural basis of 14-3-3 protein functions. Semin Cell Dev Biol. 2011;22(7):663–72.PubMedGoogle Scholar
  82. Oda Y, Fukuda H. Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science. 2012;337(6100):1333–6.PubMedGoogle Scholar
  83. Oda Y, Fukuda H. The dynamic interplay of plasma membrane domains and cortical microtubules in secondary cell wall patterning. Front Plant Sci. 2013;4:511.PubMedCentralPubMedGoogle Scholar
  84. Oda Y, Iida Y, Kondo Y, Fukuda H. Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol. 2010;20(13):1197–202.PubMedGoogle Scholar
  85. Paredez AR, Somerville CR, Ehrhardt DW. Visualization of cellulose synthase demonstrates functional association with microtubules. Science. 2006;312(5779):1491–5.PubMedGoogle Scholar
  86. Potocky M, Jones MA, Bezvoda R, Smirnoff N, Zarsky V. Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol. 2007;174(4):742–51.PubMedGoogle Scholar
  87. Qiu JL, Jilk R, Marks MD, Szymanski DB. The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell. 2002;14(1):101–18.PubMedCentralPubMedGoogle Scholar
  88. Richter S, Muller LM, Stierhof YD, Mayer U, Takada N, Kost B, Vieten A, Geldner N, Koncz C, Jurgens G. Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat Cell Biol. 2012;14(1):80–6.Google Scholar
  89. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 2006;16(10):522–9.PubMedGoogle Scholar
  90. Riou P, Kjaer S, Garg R, Purkiss A, George R, Cain RJ, Bineva G, Reymond N, McColl B, Thompson AJ, O’Reilly N, McDonald NQ, Parker PJ, Ridley AJ. 14-3-3 proteins interact with a hybrid prenyl-phosphorylation motif to inhibit G proteins. Cell. 2013;153(3):640–53.PubMedCentralPubMedGoogle Scholar
  91. Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zazimalova E, Friml J. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell. 2010;143(1):111–21.PubMedCentralPubMedGoogle Scholar
  92. Rojas AM, Fuentes G, Rausell A, Valencia A. The Ras protein superfamily: evolutionary tree and role of conserved amino acids. J Cell Biol. 2012;196(2):189–201.PubMedCentralPubMedGoogle Scholar
  93. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R. Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell. 2004;16(3):616–28.PubMedCentralPubMedGoogle Scholar
  94. Schaefer A, Hohner K, Berken A, Wittinghofer A. The unique plant RhoGAPs are dimeric and contain a CRIB motif required for affinity and specificity towards cognate small G proteins. Biopolymers. 2011a;95(6):420–33.PubMedGoogle Scholar
  95. Schaefer A, Miertzschke M, Berken A, Wittinghofer A. Dimeric plant RhoGAPs are regulated by its CRIB effector motif to stimulate a sequential GTP hydrolysis. J Mol Biol. 2011b;411(4):808–22.PubMedGoogle Scholar
  96. Schmidt A, Hall A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 2002;16(13):1587–609.PubMedGoogle Scholar
  97. Shiu SH, Bleecker AB. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE. 2001;2001(113):re22.PubMedGoogle Scholar
  98. Sorek N, Poraty L, Sternberg H, Bar E, Lewinsohn E, Yalovsky S. Activation status-coupled transient S acylation determines membrane partitioning of a plant Rho-related GTPase. Mol Cell Biol. 2007;27(6):2144–54.PubMedCentralPubMedGoogle Scholar
  99. Sorek N, Bloch D, Yalovsky S. Protein lipid modifications in signaling and subcellular targeting. Curr Opin Plant Biol. 2009;12(6):714–20.PubMedGoogle Scholar
  100. Sorek N, Segev O, Gutman O, Bar E, Richter S, Poraty L, Hirsch JA, Henis YI, Lewinsohn E, Jurgens G, Yalovsky S. An S-acylation switch of conserved G domain cysteines is required for polarity signaling by ROP GTPases. Curr Biol. 2010;20(10):914–20.PubMedGoogle Scholar
  101. Sorek N, Gutman O, Bar E, Abu-Abied M, Feng X, Running MP, Lewinsohn E, Ori N, Sadot E, Henis YI, Yalovsky S. Differential effects of prenylation and S-acylation on type I and II ROPS membrane interaction and function. Plant Physiol. 2011;155(2):706–20.PubMedCentralPubMedGoogle Scholar
  102. Sormo CG, Leiros I, Brembu T, Winge P, Os V, Bones AM. The crystal structure of Arabidopsis thaliana RAC7/ROP9: the first RAS superfamily GTPase from the plant kingdom. Phytochemistry. 2006;67(21):2332–40.PubMedGoogle Scholar
  103. Stradal TE, Scita G. Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol. 2006;18(1):4–10.PubMedGoogle Scholar
  104. Szymanski DB. Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol. 2005;8(1):103–12.PubMedGoogle Scholar
  105. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. Local positive feedback regulation determines cell shape in root hair cells. Science. 2008;319(5867):1241–4.PubMedGoogle Scholar
  106. Tcherkezian J, Lamarche-Vane N. Current knowledge of the large RhoGAP family of proteins. Biol Cell. 2007;99(2):67–86.PubMedGoogle Scholar
  107. Thapar R, Karnoub AE, Campbell SL. Structural and biophysical insights into the role of the insert region in Rac1 function. Biochemistry. 2002;41(12):3875–83.PubMedGoogle Scholar
  108. Thomas C, Berken A. Purification, crystallization and preliminary X-ray diffraction analysis of the plant Rho protein ROP5. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2007;63(Pt 12):1070–2.PubMedCentralPubMedGoogle Scholar
  109. Thomas C, Fricke I, Scrima A, Berken A, Wittinghofer A. Structural evidence for a common intermediate in small G protein-GEF reactions. Mol Cell. 2007;25(1):141–9.PubMedGoogle Scholar
  110. Thomas C, Fricke I, Weyand M, Berken A. 3D structure of a binary ROP-PRONE complex: the final intermediate for a complete set of molecular snapshots of the RopGEF reaction. Biol Chem. 2009;390(5–6):427–35.PubMedGoogle Scholar
  111. Thompson BJ. Cell polarity: models and mechanisms from yeast, worms and flies. Development. 2013;140(1):13–21.PubMedGoogle Scholar
  112. Ueda T, Kikuchi A, Ohga N, Yamamoto J, Takai Y. 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. 1990;265(16):9373–80.PubMedGoogle Scholar
  113. Uhrig JF, Mutondo M, Zimmermann I, Deeks MJ, Machesky LM, Thomas P, Uhrig S, Rambke C, Hussey PJ, Hulskamp M. The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis. Development. 2007;134(5):967–77.PubMedGoogle Scholar
  114. van Gisbergen PA, Li M, Wu SZ, Bezanilla M. Class II formin targeting to the cell cortex by binding PI(3,5)P(2) is essential for polarized growth. J Cell Biol. 2012;198(2):235–50.PubMedCentralPubMedGoogle Scholar
  115. Vetter IR, Wittinghofer A. The guanine nucleotide-binding switch in three dimensions. Science. 2001;294(5545):1299–304.PubMedGoogle Scholar
  116. Wang C, Yan X, Chen Q, Jiang N, Fu W, Ma B, Liu J, Li C, Bednarek SY, Pan J. Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. Plant Cell. 2013;25(2):499–516.PubMedCentralPubMedGoogle Scholar
  117. Wennerberg K, Der CJ. Rho-family GTPases: it’s not only Rac and Rho (and I like it). J Cell Sci. 2004;117(Pt 8):1301–12.PubMedGoogle Scholar
  118. Wennerberg K, Rossman KL, Der CJ. The Ras superfamily at a glance. J Cell Sci. 2005;118(Pt 5):843–6.PubMedGoogle Scholar
  119. Winge P, Brembu T, Bones A. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol Biol. 1997;35(4):483–95.PubMedGoogle Scholar
  120. Winge P, Brembu T, Kristensen R, Bones AM. Genetic structure and evolution of RAC-GTPases in Arabidopsis thaliana. Genetics. 2000;156(4):1959–71.PubMedCentralPubMedGoogle Scholar
  121. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell. 2007;19(12):4022–34.PubMedCentralPubMedGoogle Scholar
  122. Wu G, Li H, Yang Z. 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;124(4):1625–36.PubMedCentralPubMedGoogle Scholar
  123. Wu G, Gu Y, Li S, Yang Z. A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell. 2001;13(12):2841–56.PubMedCentralPubMedGoogle Scholar
  124. Wu Y, Zhao S, Tian H, He Y, Xiong W, Guo L, Wu Y. CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells. J Exp Bot. 2013;64(11):3327–38.PubMedCentralPubMedGoogle Scholar
  125. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z. Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell. 2010;143(1):99–110.PubMedCentralPubMedGoogle Scholar
  126. Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusova H, Wang W, Jones AM, Friml J, Patterson SE, Bleecker AB, Yang Z. Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science. 2014;343(6174):1025–8.PubMedCentralPubMedGoogle Scholar
  127. Yalovsky S, Bloch D, Sorek N, Kost B. Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol. 2008;147(4):1527–43.PubMedCentralPubMedGoogle Scholar
  128. Zhang Y, McCormick S. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2007;104(47):18830–5.PubMedCentralPubMedGoogle Scholar
  129. Zhang X, Bi E, Novick P, Du L, Kozminski KG, Lipschutz JH, Guo W. Cdc42 interacts with the exocyst and regulates polarized secretion. J Biol Chem. 2001;276(50):46745–50.PubMedGoogle Scholar
  130. Zhang C, Kotchoni SO, Samuels AL, Szymanski DB. SPIKE1 signals originate from and assemble specialized domains of the endoplasmic reticulum. Curr Biol. 2010;20(23):2144–9.PubMedGoogle Scholar
  131. Zhang C, Halsey LE, Szymanski DB. The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol. 2011;11:27.PubMedCentralPubMedGoogle Scholar
  132. Zhang C, Mallery E, Reagan S, Boyko VP, Kotchoni SO, Szymanski DB. The endoplasmic reticulum is a reservoir for WAVE/SCAR regulatory complex signaling in the Arabidopsis leaf. Plant Physiol. 2013a;162(2):689–706.PubMedCentralPubMedGoogle Scholar
  133. Zhang C, Mallery EL, Szymanski DB. ARP2/3 localization in Arabidopsis leaf pavement cells: a diversity of intracellular pools and cytoskeletal interactions. Front Plant Sci. 2013b;4:238.PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Daria Bloch
    • 1
  • Gil Feiguelman
    • 1
  • Ella Buriakovsky
    • 1
  • Shaul Yalovsky
    • 1
  1. 1.Department of Molecular Biology and Ecology of PlantsTel Aviv UniversityTel AvivIsrael

Personalised recommendations