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Emerging Roles of Rho GTPases in Plants

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GTPases

Part of the book series: SpringerBriefs in Plant Science ((BRIEFSPLANT))

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Abstract

The animal Ras/Rho-related GTPas gene family is represented by a sole family of ROP proteins in plants. Plant ROPs presumably interact with cell surface receptors in response to specific stimuli including abiotic, biotic, and hormonal elicitors to mediate diverse signaling responses. There are both similarities and at the same time differences at the regulatory level in plant versus non-plant Rho GTPases. ROPs are apparently capable of interacting with multiple effector molecules affecting several cellular biochemical responses such as actin dynamics, protein degradation, and interaction with the environment. ROPs are thus regarded as multifunctional proteins that integrate several cellular signals and coordinate diverse pathways to regulate growth, development, and stress responses.

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References

  1. Lowy DR, Willumsen BM. Function and regulation of ras. Annu Rev Biochem. 1993;62:851–91.

    Article  CAS  PubMed  Google Scholar 

  2. Terryn N, Van Montagu M, Inze D. GTP-binding proteins in plants. Plant Mol Biol. 1993;22(1):143–52.

    Article  CAS  PubMed  Google Scholar 

  3. Assmann SM. Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell. 2002;14(Suppl):S355–73.

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, et al. The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell. 2003;15(2):393–409.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Zheng ZL, Yang Z. The RopGTPase: an emerging signaling switch in plants. Plant Mol Biol. 2000;44:1–9.

    Article  CAS  PubMed  Google Scholar 

  6. Zheng ZL, Nafisi M, Tam A, Li H, Crowell DN, Chary SN, et al. Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell. 2002;14(11):2787–97.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Tao LZ, Cheung AY, Wu HM. Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell. 2002;14(11):2745–60.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. Schultheiss H, Dechert C, Kogel KH, Huckelhoven R. Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J. 2003;36(5):589–601.

    Article  CAS  PubMed  Google Scholar 

  10. Poraty-Gavra L, Zimmermann P, Haigis S, Bednarek P, Hazak O, Stelmakh OR, et al. The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways. Plant Physiol. 2013;161(3):1172–88.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K. Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci U S A. 2001;98(2):759–64.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell. 2007;19(12):4022–34.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Thao NP, Chen L, Nakashima A, Hara S, Umemura K, Takahashi A, et al. RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. Plant Cell. 2007;19(12):4035–45.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, et al. Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol. 2010;51(4):585–95.

    Article  CAS  PubMed  Google Scholar 

  15. Hoefle C, Huesmann C, Schultheiss H, Börnke F, Hensel G, Kumlehn J, et al. 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;23:2422–39.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Jung YH, Agrawal GK, Rakwal R, Kim JA, Lee MO, Choi PG, et al. Functional characterization of OsRacB GTPase-a potentially negative regulator of basal disease resistance in rice. Plant Physiol Biochem. 2006;44(1):68–77.

    Article  CAS  PubMed  Google Scholar 

  17. Nibau C, Wu HM, Cheung AY. RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trends Plant Sci. 2006;11(6):309–15.

    Article  CAS  PubMed  Google Scholar 

  18. Yang Z, Fu Y. ROP/RAC GTPase signaling. Curr Opin Plant Biol. 2007;10(5):490–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–33.

    Article  CAS  PubMed  Google Scholar 

  20. Grunewald W, Friml J. The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J. 2010;29(16):2700–14.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, et al. ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci U S A. 2010;107(50):21890–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Tanaka H, Kitakura S, Rakusova H, Uemura T, Feraru MI, De Rycke R, et al. Cell polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis thaliana. PLoS Genet. 2013;9(5):e1003540.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Smith LG, Oppenheimer DG. Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol. 2005;21:271–95.

    Article  CAS  PubMed  Google Scholar 

  24. Hussey PJ, Ketelaar T, Deeks MJ. Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol. 2006;57:109–25.

    Article  CAS  PubMed  Google Scholar 

  25. Dong CH, Xia GX, Hong Y, Ramachandran S, Kost B, Chua NH. ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell. 2001;13(6):1333–46.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Cardenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK. Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol. 2008;146(4):1611–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, et al. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 2001;20(11):2779–88.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, et al. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Bloch D, Monshausen G, Gilroy S, Yalovsky S. Co-regulation of root hair tip growth by ROP GTPases and nitrogen source modulated pH fluctuations. Plant Signal Behav. 2011;6(3):426–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, et al. A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol. 2007;17(11):947–52.

    Article  CAS  PubMed  Google Scholar 

  35. Zhang X, Orlando K, He B, Xi F, Zhang J, Zajac A, et al. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J Cell Biol. 2008;180(1):145–58.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Elias M, Drdova E, Ziak D, Bavlnka B, Hala M, Cvrckova F, et al. The exocyst complex in plants. Cell Biol Int. 2003;27:199–201.

    Article  CAS  PubMed  Google Scholar 

  37. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, et al. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell. 2008;20(5):1330–45.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS. The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol. 2005;138(3):1637–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Orlando K, Guo W. Membrane organization and dynamics in cell polarity. Cold Spring Harb Perspect Biol. 2009;1(5):a001321.

    Article  PubMed Central  PubMed  Google Scholar 

  40. Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, et al. Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity. Curr Biol. 2006;16:2143–9.

    Article  CAS  PubMed  Google Scholar 

  41. Lee YJ, Yang Z. Tip growth: signaling in the apical dome. Curr Opin Plant Biol. 2008;11(6):662–71.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Yang Z, Lavagi I. Spatial control of plasma membrane domains: ROP GTPase-based symmetry breaking. Curr Opin Plant Biol. 2012;15(6):601–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Li H, Lin Y, Heath RM, Zhu MX, Yang Z. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell. 1999;11(9):1731–42.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, et al. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Lee YJ, Szumlanski A, Nielsen E, Yang Z. Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J Cell Biol. 2008;181(7):1155–68.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. 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.

    Article  CAS  PubMed  Google Scholar 

  48. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Clarkson D. Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol. 1985;36:77–115.

    Article  CAS  Google Scholar 

  50. Bauer WD. Infection of legumes by rhizobia. Annu Rev Plant Physiol. 1981;32:407–49.

    Article  CAS  Google Scholar 

  51. Eaton S, Wepf R, Simons K. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J Cell Biol. 1996;135(5):1277–89.

    Article  CAS  PubMed  Google Scholar 

  52. Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, et al. 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;227(2):618–32.

    Article  CAS  PubMed  Google Scholar 

  53. Ziman M, Preuss D, Mulholland J, O’Brien JM, Botstein D, Johnson DI. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol Biol Cell. 1993;4(12):1307–16.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Yamochi W, Tanaka K, Nonaka H, Maeda A, Musha T, Takai Y. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J Cell Biol. 1994;125(5):1077–93.

    Article  CAS  PubMed  Google Scholar 

  55. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science. 1999;286(5438):316–8.

    Article  CAS  PubMed  Google Scholar 

  56. Bloch D, Lavy M, Efrat Y, Efroni I, Bracha-Drori K, Abu-Abied M, et al. Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol Biol Cell. 2005;16(4):1913–27.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. 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.

    Article  CAS  PubMed  Google Scholar 

  58. Yang Z. Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol. 2008;24:551–75.

    Article  PubMed Central  PubMed  Google Scholar 

  59. Fu Y, Li H, Yang Z. 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;14(4):777–94.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Badescu GO, Napier RM. Receptors for auxin: will it all end in TIRs? Trends Plant Sci. 2006;11(5):217–23.

    Article  CAS  PubMed  Google Scholar 

  61. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, et al. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell. 2010;143:99–110.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Fu Y, Xu T, Zhu L, Wen M, Yang Z. A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol. 2009;19(21):1827–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Pandey, G.K., Sharma, M., Pandey, A., Shanmugam, T. (2015). Emerging Roles of Rho GTPases in Plants. In: GTPases. SpringerBriefs in Plant Science. Springer, Cham. https://doi.org/10.1007/978-3-319-11611-2_6

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