New insights into Rho signaling from plant ROP/Rac GTPases

Trends in Cell Biology

Volumn 22, Issue 9, 2012, Pages 492-501

  Craddock, Christian ^a   Lavagi, Irene ^a   Yang, Zhenbiao ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLATHRIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; RHO FACTOR;

ANIMAL; CELL MEMBRANE; CELL POLARITY; ENDOCYTOSIS; EXOCYTOSIS; MICROFILAMENT; MICROTUBULE; NONHUMAN; PLANT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; YEAST;

ANIMALS; GTP PHOSPHOHYDROLASES; HUMANS; PLANTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 84865589055     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2012.05.002     Document Type: Review

References (98)

1. Chant J., Stowers L. GTPase cascades choreographing cellular behavior: movement, morphogenesis, and more. Cell 1995, 81:1-4.
2. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
3. Yang Z., Watson J.C. 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, 90:8732-8736.
4. Li H., et al. Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol. 1998, 118:407-417.
5. Winge P., et al. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol. Biol. 1997, 35:483-495.
6. Vernoud V., et al. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 2003, 131:1191-1208.
7. Yang Z. Small GTPases: versatile signaling switches in plants. Plant Cell 2002, 14(Suppl.):S375-S388.
8. Eklund D.M., et al. Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth. J. Exp. Bot. 2010, 61:1917-1937.
9. Lagana A., et al. A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat. Cell Biol. 2010, 12:1186-1193.
10. Li H., et al. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 1999, 11:1731-1742.
11. Kost B., 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, 145:317-330.
12. Gu Y., et al. ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J. Exp. Bot. 2003, 54:93-101.
13. Yang G., et al. A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS ONE 2007, 2:e1074.
14. Molendijk A.J., et al. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 2001, 20:2779-2788.
15. Jones M.A., et al. NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J. Exp. Bot. 2007, 58:1261-1270.
16. Duan Q., et al. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17821-17826.
17. Yoo C.M., et al. AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J. 2012, 69:1064-1076.
18. Ohta Y., et al. FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling. Nat. Cell Biol. 2006, 8:803-814.
19. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9:690-701.
20. Berken A. ROPs in the spotlight of plant signal transduction. Cell. Mol. Life Sci. 2006, 63:2446-2459.
21. Brembu T., et al. A RHOse by any other name: a comparative analysis of animal and plant Rho GTPases. Cell Res. 2006, 16:435-445.
22. Wu G., et al. A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 2001, 13:2841-2856.
23. Li S., et al. 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, 1:1021-1035.
24. Lavy M., et al. A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 2007, 17:947-952.
25. Fu Y., et al. A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr. Biol. 2009, 19:1827-1832.
26. Ehrhardt D.W., Shaw S.L. Microtubule dynamics and organization in the plant cortical array. Annu. Rev. Plant Biol. 2006, 57:859-875.
27. Staiger C.J., Blanchoin L. Actin dynamics: old friends with new stories. Curr. Opin. Plant Biol. 2006, 9:554-562.
28. Staiger C.J., et al. Regulation of actin dynamics by actin-binding proteins in pollen. J. Exp. Bot. 2010, 61:1969-1986.
29. Yang Z. Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 2008, 24:551-575.
30. Lee Y.J., Yang Z. Tip growth: signaling in the apical dome. Curr. Opin. Plant Biol. 2008, 11:662-671.
31. Mucha E., et al. Rho proteins of plants--functional cycle and regulation of cytoskeletal dynamics. Eur. J. Cell Biol. 2011, 90:934-943.
32. Gu Y., et al. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 2005, 169:127-138.
33. Fuchs U., et al. Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol. Biol. Cell 2005, 16:2746-2758.
34. Mourino-Perez R.R., et al. Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet. Biol. 2006, 43:389-400.
35. Raudaskoski M., et al. Microtubule cytoskeleton in hyphal growth. Response to nocodazole in a sensitive and a tolerant strain of the homobasidiomycete Schizophyllum commune. Eur. J. Cell Biol. 1994, 64:131-141.
36. Nakamura M., et al. Arabidopsis GCP3-interacting protein 1/MOZART1 is an integral component of the gamma-tubulin-containing microtubule nucleating complex. Plant J. 2012, 71:216-225.
37. Shaw S.L., et al. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 2003, 300:1715-1718.
38. Wasteneys G.O., Ambrose J.C. Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol. 2009, 19:62-71.
39. Fu Y., et al. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 2005, 120:687-700.
40. Xu T., et al. Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 2010, 143:99-110.
41. Brennwald P., Rossi G. Spatial regulation of exocytosis and cell polarity: yeast as a model for animal cells. FEBS Lett. 2007, 581:2119-2124.
42. France Y.E., et al. The polarity-establishment component Bem1p interacts with the exocyst complex through the Sec15p subunit. J. Cell Sci. 2006, 119:876-888.
43. Mehta S.Q., et al. Mutations in Drosophila sec15 reveal a function in neuronal targeting for a subset of exocyst components. Neuron 2005, 46:219-232.
44. Wedlich-Soldner R., et al. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 2004, 166:889-900.
45. Zajac A., et al. Cyclical regulation of the exocyst and cell polarity determinants for polarized cell growth. Mol. Biol. Cell 2005, 16:1500-1512.
46. Guo W., et al. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 2001, 3:353-360.
47. Zhang X., et al. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 2001, 276:46745-46750.
48. Cole R.A., Fowler J.E. Polarized growth: maintaining focus on the tip. Curr. Opin. Plant Biol. 2006, 9:579-588.
49. Hazak O., et al. A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 2010, 8:e1000282.
50. Mravec J., et al. Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr. Biol. 2011, 21:1055-1060.
51. Richter S., et al. Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat. Cell Biol. 2012, 14:80-86.
52. Nagawa S., et al. RHO GTPase in plants: conservation and invention of regulators and effectors. Small Gtpases 2010, 1:78-88.
53. Lee Y.J., et al. Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 2008, 181:1155-1168.
54. Zhao Y., et al. Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. Plant Cell 2010, 22:4031-4044.
55. Shivas J.M., et al. Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 2010, 20:445-452.
56. Izumi G., et al. Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. J. Cell Biol. 2004, 166:237-248.
57. Harris K.P., Tepass U. Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J. Cell Biol. 2008, 183:1129-1143.
58. Nagawa S., et al. ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 2012, 10:e1001299.
59. Paciorek T., et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 2005, 435:1251-1256.
60. Xu T., et al. Uniform auxin triggers the Rho GTPase-dependent formation of interdigitation patterns in pavement cells. Small Gtpases 2011, 2:227-232.
61. Kaksonen M., et al. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2006, 7:404-414.
62. Yarar D., et al. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol. Biol. Cell 2005, 16:964-975.
63. Anitei M., Hoflack B. Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat. Cell Biol. 2012, 14:11-19.
64. Berken A., et al. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 2005, 436:1176-1180.
65. Gu Y., et al. Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. Plant Cell 2006, 18:366-381.
66. Basu D., et al. 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, 105:4044-4049.
67. Wu G., et al. 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, 124:1625-1636.
68. Hwang J.U., et al. A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr. Biol. 2008, 18:1907-1916.
69. Klahre U., et al. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J. 2006, 46:1018-1031.
70. Lin Y., et al. Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 1996, 8:293-303.
71. Fodor-Dunai C., et al. The phosphomimetic mutation of an evolutionarily conserved serine residue affects the signaling properties of Rho of plants (ROPs). Plant J. 2011, 66:669-679.
72. Berken A., Wittinghofer A. Structure and function of Rho-type molecular switches in plants. Plant Physiol. Biochem. 2008, 46:380-393.
73. Ivanchenko M., et al. Maize ROP7 GTPase contains a unique, CaaX box-independent plasma membrane targeting signal. Plant J. 2000, 24:79-90.
74. Lavy M., et al. A cell-specific, prenylation-independent mechanism regulates targeting of type II RACs. Plant Cell 2002, 14:2431-2450.
75. 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, 46:934-947.
76. Sorek N., et al. Activation status-coupled transient S acylation determines membrane partitioning of a plant Rho-related GTPase. Mol. Cell. Biol. 2007, 27:2144-2154.
77. Sorek N., et al. An S-acylation switch of conserved G domain cysteines is required for polarity signaling by ROP GTPases. Curr. Biol. 2010, 20:914-920.
78. Brugnera E., et al. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 2002, 4:574-582.
79. Meller N., et al. Zizimin1, a novel Cdc42 activator, reveals a new GEF domain for Rho proteins. Nat. Cell Biol. 2002, 4:639-647.
80. Yamaguchi K., et al. SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J. 2011, 70:389-397.
81. 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, 104:18830-18835.
82. Cheung A.Y., et al. The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule-binding reporter proteins. Mol. Plant 2008, 1:686-702.
83. Nibau C., Cheung A.Y. New insights into the functional roles of CrRLKs in the control of plant cell growth and development. Plant Signal. Behav. 2011, 6:655-659.
84. Kessler S.A., et al. Conserved molecular components for pollen tube reception and fungal invasion. Science 2010, 330:968-971.
85. Humphries J.A., et al. ROP GTPases act with the receptor-like protein PAN1 to polarize asymmetric cell division in maize. Plant Cell 2011, 23:2273-2284.
86. Chen M., et al. RopGEF7 regulates PLETHORA-dependent maintenance of the root stem cell niche in Arabidopsis. Plant Cell 2011, 23:2880-2894.
87. Hwang J.U., et al. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol. Biol. Cell 2005, 16:5385-5399.
88. Hwang J.U., et al. Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J. Cell Sci. 2010, 123:340-350.
89. Myers C., et al. Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J. 2009, 59:528-539.
90. Qin Y., Yang Z. Rapid tip growth: insights from pollen tubes. Semin. Cell Dev. Biol. 2011, 22:816-824.
91. Yan A., et al. Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:22002-22007.
92. Jenkins N., et al. CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 2006, 313:1298-1301.
93. Saito K., et al. Transbilayer phospholipid flipping regulates Cdc42p signaling during polarized cell growth via Rga GTPase-activating proteins. Dev. Cell 2007, 13:743-751.
94. Anderson D.C., et al. Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts. Science 2008, 320:1771-1774.
95. Klahre U., Kost B. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 2006, 18:3033-3046.
96. Zhang C., et al. SPIKE1 signals originate from and assemble specialized domains of the endoplasmic reticulum. Curr. Biol. 2010, 20:2144-2149.
97. Kawano Y., et al. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity. Cell Host Microbe 2010, 7:362-375.
98. Harris K.P., Tepass U. Cdc42 and vesicle trafficking in polarized cells. Traffic 2010, 11:1272-1279.