CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells

Journal of Experimental Botany

Volumn 64, Issue 11, 2013, Pages 3327-3338

  Wu, Yuxuan ^a   Zhao, Shujuan ^a   Tian, Han ^a   He, Yuqing ^a   Xiong, Wei ^a   Guo, Lin ^a   Wu, Yan ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Calcium; CPK3; GDI1; pavement cells; phosphorylation; ROP.

Indexed keywords

ARABIDOPSIS PROTEIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CPK3 PROTEIN, ARABIDOPSIS; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1;

ARABIDOPSIS; ARTICLE; CPK3; CYTOLOGY; GDI1; GENETICS; METABOLISM; PAVEMENT CELLS; PHOSPHORYLATION; PHYSIOLOGY; PLANT EPIDERMIS; PLANT LEAF; ROP.; SEEDLING; SIGNAL TRANSDUCTION;

CALCIUM; CPK3; GDI1; PAVEMENT CELLS; PHOSPHORYLATION; ROP.;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; PHOSPHORYLATION; PLANT EPIDERMIS; PLANT LEAVES; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; SEEDLING; SIGNAL TRANSDUCTION;

EID: 84882366054     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert171     Document Type: Article

References (52)

1. Alonso JM, Stepanova AN, Leisse TJ, et al. 2003. Genomewide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
2. Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB. 2008. A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proceedings of the National Academy of Sciences, USA 105, 4044-4049.
3. Baxter-Burrell A, Yang ZB, Springer PS, Bailey-Serres J. 2002. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296, 2026-2028.
4. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602.
5. Berken A, Thomas C, Wittinghofer A. 2005. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 436, 1176-1180.
6. Bischoff F, Vahlkamp L, Molendijk A, Palme K. 2000. Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Molecular Biology 42, 515-530.
7. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan LB, He P, Bush J, Cheng SH, Sheen J. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464, 418-422.
8. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K. 2010. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nature Cell Biology 12, 477-483.
9. 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.
10. Chen X, Wu D, Zhao Y, Wong BHC, Guo L. 2011. Increasing phosphoproteome coverage and identification of phosphorylation motifs through combination of different HPLC fractionation methods. Journal of Chromatography B 879, 25-34.
11. Cheng SH, Willmann MR, Chen HC, Sheen J. 2002. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiology 129, 469-485.
12. DerMardirossian C, Schnelzer A, Bokoch GM. 2004. Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Molecular Cell 15, 117-127.
13. Dransart E, Olofsson B, Cherfils J. 2005. RhoGDIs revisited: novel roles in Rho regulation. Traffic 6, 957-966.
14. Engstrom EM, Ehrhardt DW, Mitra RM, Long SR. 2002. Pharmacological analysis of nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiology 128, 1390-1401.
15. Fu Y, Gu Y, Zheng ZL, Wasteneys G, Yang ZB. 2005. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120, 687-700.
16. Fu Y, Li H, Yang ZB. 2002. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. The Plant Cell 14, 777-794.
17. Fu Y, Wu G, Yang ZB. 2001. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. Journal of Cell Biology 152, 1019-1032.
18. Fu Y, Xu TD, Zhu L, Wen MZ, Yang ZB. 2009. A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Current Biology 19, 1827-1832.
19. Fu Y, Yang ZB. 2001. Rop GTPase: a master switch of cell polarity development in plants. Trends in Plant Science 6, 545-547.
20. Garcia-Mata R, Boulter E, Burridge K. 2011. The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nature Reviews Molecular Cell Biology 12, 493-504.
21. Geiger D, Scherzer S, Mumm P, et al. 2010. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proceedings of the National Academy of Sciences, USA 107, 8023-8028.
22. Gu Y, Li SD, Lord EM, Yang ZB. 2006. Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control rho GTPase-dependent polar growth. The Plant Cell 18, 366-381.
23. Hwang JU, Vernoud V, Szumlanski A, Nielsen E, Yang ZB. 2008. A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Current Biology 18, 1907-1916.
24. Hwang JU, Wu G, Yan A, Lee YJ, Grierson CS, Yang ZB. 2010. Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. Journal of Cell Science 123, 340-350.
25. Ivashuta S, Liu JY, Liu JQ, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS. 2005. RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. The Plant Cell 17, 2911-2921.
26. Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miège C, Gaude T. 2007. The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130, 1057-1070.
27. Kaothien P, Ok SH, Shuai B, Wengier D, Cotter R, Kelley D, Kiriakopolos S, Muschietti J, McCormick S. 2005. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. The Plant Journal 42, 492-503.
28. Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H. 2006. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. The Plant Cell 18, 2733-2748.
29. Klahre U, Becker C, Schmitt AC, Kost B. 2006. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. The Plant Journal 46, 1018-1031.
30. Klahre U, Kost B. 2006. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. The Plant Cell 18, 3033-3046.
31. Kost B. 2008. Spatial control of Rho (Rac-Rop) signaling in tipgrowing plant cells. Trends in Cell Biology 18, 119-127.
32. Kraynov VS, Chamberlain C, Bokoch GM, Schwartz MA, Slabaugh S, Hahn KM. 2000. Localized Rac activation dynamics visualized in living cells. Science 290, 333-337.
33. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S. 2007. A novel ROP/RAC effector links cell polarity, root-meristern maintenance, and vesicle trafficking. Current Biology 17, 947-952.
34. Le J, Mallery EL, Zhang CH, Brankle S, Szymanski DB. 2006. Arabidopsis BRICK1/HSPC300 is an essential WAVE-complex subunit that selectively stabilizes the Arp2/3 activator SCAR2. Current Biology 16, 895-901.
35. Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH. 2001. Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes and Development 15, 1808-1816.
36. Mehlmer N, Wurzinger B, Stael S, Hofmann-Rodrigues D, Csaszar E, Pfister B, Bayer R, Teige M. 2010. The Ca2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. The Plant Journal 63, 484-498.
37. Mori IC, Murata Y, Yang YZ, et al. 2006. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion-and Ca2+-permeable channels and stomatal closure. PLoS Biology 4, 1749-1762.
38. Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF. 2009. Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. The Plant Journal 59, 528-539.
39. Romeis T, Piedras P, Jones JDG. 2000. Resistance genedependent activation of a calcium-dependent protein kinase in the plant defense response. The Plant Cell 12, 803-815.
40. Sorek N, Gutman O, Bar E, et al. 2011. Differential effects of prenylation and s-acylation on type I and II ROPS membrane interaction and function. Plant Physiology 155, 706-720.
41. Tao LZ, Cheung AY, Nibau C, Wu HM. 2005. RAC GTPases in tobacco and Arabidopsis mediate auxin-induced formation of proteolytically active nuclear protein bodies that contain AUX/IAA proteins. The Plant Cell 17, 2369-2383.
42. Tao LZ, Cheung AY, Wu HM. 2002. Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. The Plant Cell 14, 2745-2760.
43. Walter M, Chaban C, Schutze K, et al. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428-438.
44. Wang YP, Li L, Ye TT, Zhao SJ, Liu Z, Feng YQ, Wu Y. 2011. Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. The Plant Journal 68, 249-261.
45. Wong HL, Pinontoan R, Hayashi K, et al. 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. The Plant Cell 19, 4022-4034.
46. Wu G, Gu Y, Li SD, Yang ZB. 2001. A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. The Plant Cell 13, 2841-2856.
47. Wu G, Li H, Yang ZB. 2000. Arabidopsis RopGAPs are a novel family of Rho GTPase-activating proteins that require the Cdc42/Racinteractive binding motif for Rop-specific GTPase stimulation. Plant Physiology 124, 1625-1636.
48. Xu TD, Wen MZ, Nagawa S, et al. 2010. Cell surface-and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110.
49. Yang ZB. 2008. Cell polarity signaling in Arabidopsis. Annual Review of Cell and Developmental Biology 24, 551-575.
50. Yoon GM, Dowd PE, Gilroy S, McCubbin AG. 2006. Calciumdependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. The Plant Cell 18, 867-878.
51. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N, Nagashima K, Matsuda M. 2003. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. Journal of Cell Biology 162, 223-232.
52. Zhang C, Halsey LE, Szymanski DB. 2011. The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biology 11, 27.