Recruitment of PLANT U-BOX13 and the PI4Kβ1/β2 phosphatidylinositol-4 kinases by the small GTPase RabA4B plays important roles during salicylic acid-mediated plant defense signaling in arabidopsis

Plant Cell

Volumn 27, Issue 1, 2015, Pages 243-261

  Antignani, Vincenzo ^a   Klocko, Amy L ^a   Bak, Gwangbae ^a   Chandrasekaran, Suma D ^a   Dunivin, Taylor ^a   Nielsen, Erik ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARMADILLO; EUKARYOTA;

ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK;

EID: 84923066872     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.134262     Document Type: Article

References (83)

1. Aravind, L., and Koonin, E.V. (2000). The U box is a modified RING finger—A common domain in ubiquitination. Curr. Biol. 10: R132–R134.
2. Audhya, A., Foti, M., and Emr, S.D. (2000). Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell 11: 2673–2689.
3. Bae, H., and Kim, W.T. (2013). The N-terminal tetra-peptide (IPDE) short extension of the U-box motif in rice SPL11 E3 is essential for the interaction with E2 and ubiquitin-ligase activity. Biochem. Bio-phys. Res. Commun. 433: 266–271.
4. Bardoel, B.W., van der Ent, S., Pel, M.J.C., Tommassen, J., Pieterse, C.M.J., van Kessel, K.P.M., and van Strijp, J.A.G. (2011). Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7: e1002206.
5. Beck, M., Zhou, J., Faulkner, C., MacLean, D., and Robatzek, S. (2012). Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24: 4205–4219.
6. Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F., and Dong, X. (1994). A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6: 1845–1857.
7. Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and Felix, G. (2006). The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465–476.
8. Choi, S.-W., Tamaki, T., Ebine, K., Uemura, T., Ueda, T., and Nakano, A. (2013). RABA members act in distinct steps of sub-cellular trafficking of the FLAGELLIN SENSING2 receptor. Plant Cell 25: 1174–1187.
9. Christoforidis, S., McBride, H.M., Burgoyne, R.D., and Zerial, M. (1999a). The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621–625.
10. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S.-C., Waterfield, M.D., Backer, J.M., and Zerial, M. (1999b). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1: 249–252.
11. Citovsky, V., Lee, L.-Y., Vyas, S., Glick, E., Chen, M.-H., Vainstein, A., Gafni, Y., Gelvin, S.B., and Tzfira, T. (2006). Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 362: 1120–1131.
12. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.
13. Coates, J.C. (2003). Armadillo repeat proteins: Beyond the animal kingdom. Trends Cell Biol. 13: 463–471.
14. DebRoy, S., Thilmony, R., Kwack, Y.B., Nomura, K., and He, S.Y. (2004). A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc. Natl. Acad. Sci. USA 101: 9927–9932.
15. De Camilli, P., Chen, H., Hyman, J., Panepucci, E., Bateman, A., and Brunger, A.T. (2002). The ENTH domain. FEBS Lett. 513: 11–18.
16. Ellinger, D., Glöckner, A., Koch, J., Naumann, M., Stürtz, V., Schütt, K., Manisseri, C., Somerville, S.C., and Voigt, C.A. (2014). Interaction of the Arabidopsis GTPase RabA4c with its effector PMR4 results in complete penetration resistance to powdery mildew. Plant Cell 26: 3185–3200.
17. Feraru, E., Feraru, M.I., Asaoka, R., Paciorek, T., De Rycke, R., Tanaka, H., Nakano, A., and Friml, J. (2012). BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis. Plant Cell 24: 3074–3086.
18. Furt, F., König, S., Bessoule, J.-J., Sargueil, F., Zallot, R., Stanislas, T., Noirot, E., Lherminier, J., Simon-Plas, F., Heilmann, I., and Mongrand, S. (2010). Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol. 152: 2173–2187.
19. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.-D., and Chory, J. (2009). Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59: 169–178.
20. Gietz, R.D., and Woods, R.A. (1994). High efficiency transformation with lithium acetate in yeast. In Molecular Genetics of Yeast: A Practical Approach, J.R. Johnston, ed (Oxford, UK: IRL Press), pp. 121–134.
21. Godi, A., Di Campli, A., Konstantakopoulos, A., Di Tullio, G., Alessi, D.R., Kular, G.S., Daniele, T., Marra, P., Lucocq, J.M., and De Matteis, M.A. (2004). FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6: 393–404.
22. Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J.W., and Robatzek, S. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18: 1824–1832.
23. Gomez-Gomez, L., and Boller, T. (2000). FLS2: a LRR receptor-like kinase involved in recognition of the flagellin elicitor in Arabidopsis. Mol. Cell 5: 1–20.
24. Gómez-Gómez, L., Bauer, Z., and Boller, T. (2001). Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13: 1155–1163.
25. González-Lamothe, R., Tsitsigiannis, D.I., Ludwig, A.A., Panicot, M., Shirasu, K., and Jones, J.D.G. (2006). The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18: 1067–1083.
26. Grosshans, B.L., Ortiz, D., and Novick, P. (2006). Rabs and their effectors: Achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103: 11821–11827.
27. Gu, Y., Fu, Y., Dowd, P., Li, S., Vernoud, V., Gilroy, S., and Yang, Z. (2005). A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169: 127–138.
28. Haas, T.J., Sliwinski, M.K., Martínez, D.E., Preuss, M., Ebine, K., Ueda, T., Nielsen, E., Odorizzi, G., and Otegui, M.S. (2007). The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endo-some function and interacts with its positive regulator LYS-T-INTERACTING PROTEIN5. Plant Cell 19: 1295–1312.
29. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K.-I. (2001). U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276: 33111–33120.
30. Hu, C.-D., Chinenov, Y., and Kerppola, T.K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9: 789–798.
31. Hutagalung, A.H., and Novick, P.J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91: 119–149.
32. Hyman, J., Chen, H., Di Fiore, P.P., De Camilli, P., and Brunger, A.T. (2000). Epsin 1 undergoes nucleocytosolic shuttling and its eps15 in-teractor NH2-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor pro-myelocytic leukemia Zn2+ finger protein (PLZF). J. Cell Biol. 149: 537–546.
33. Ishiga, Y., Ishiga, T., Uppalapati, S.R., and Mysore, K.S. (2011). Arabi-dopsis seedling flood-inoculation technique: A rapid and reliable assay for studying plant-bacterial interactions. Plant Methods 7: 32.
34. Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S., and Takenawa, T. (2001). Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291: 1047–1051.
35. Kang, B.-H., Nielsen, E., Preuss, M.L., Mastronarde, D., and Staehelin, L.A. (2011). Electron tomography of RabA4b- and PI-4Kb1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12: 313–329.
36. Korasick, D.A., McMichael, C., Walker, K.A., Anderson, J.C., Bednarek, S.Y., and Heese, A. (2010). Novel functions of Stomatal Cytokinesis-Defective 1 (SCD1) in innate immune responses against bacteria. J. Biol. Chem. 285: 23342–23350.
37. Lee, Y., Kim, Y.-W., Jeon, B.W., Park, K.-Y., Suh, S.J., Seo, J., Kwak, J.M., Martinoia, E., Hwang, I., and Lee, Y. (2007). Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. Plant J. 52: 803–816.
38. Li, W., et al. (2012a). The U-box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol. 159: 239–250.
39. Li, W., Dai, L., and Wang, G.-L. (2012b). PUB13, a U-box/ARM E3 ligase, regulates plant defense, cell death, and flowering time. Plant Signal. Behav. 7: 898–900.
40. Li, X., Rivas, M.P., Fang, M., Marchena, J., Mehrotra, B., Chaudhary, A., Feng, L., Prestwich, G.D., and Bankaitis, V.A. (2002). Analysis of oxysterol binding protein homologue Kes1p function in regulation of Sec14p-dependent protein transport from the yeast Golgi complex. J. Cell Biol. 157: 63–77.
41. Liew, F.Y., Xu, D., Brint, E.K., and O’Neill, L.A.J. (2005). Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5: 446–458.
42. Liu, J., Li, W., Ning, Y., Shirsekar, G., Cai, Y., Wang, X., Dai, L., Wang, Z., Liu, W., and Wang, G.-L. (2012). The U-box E3 ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiol. 160: 28–37.
43. Lu, D., Lin, W., Gao, X., Wu, S., Cheng, C., Avila, J., Heese, A., Devarenne, T.P., He, P., and Shan, L. (2011). Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439–1442.
44. Mudgil, Y., Shiu, S.-H., Stone, S.L., Salt, J.N., and Goring, D.R. (2004). A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiol. 134: 59–66.
45. Mueller-Roeber, B., and Pical, C. (2002). Inositol phospholipid metabolism in Arabidopsis: Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phos-pholipase C. Plant Physiol. 130: 22–46.
46. Nielsen, E., Christoforidis, S., Uttenweiler-Joseph, S., Miaczynska, M., Dewitte, F., Wilm, M., Hoflack, B., and Zerial, M. (2000). Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to en-dosomes through a FYVE finger domain. J. Cell Biol. 151: 601–612.
47. Nishimura, M.T., Stein, M., Hou, B.-H., Vogel, J.P., Edwards, H., and Somerville, S.C. (2003). Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969–972.
48. Ohi, M.D., Vander Kooi, C.W., Rosenberg, J.A., Chazin, W.J., and Gould, K.L. (2003). Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 10: 250–255.
49. Pereira-Leal, J.B., and Seabra, M.C. (2001). Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313: 889–901.
50. Preuss, M.L., Schmitz, A.J., Thole, J.M., Bonner, H.K.S., Otegui, M.S., and Nielsen, E. (2006). A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J. Cell Biol. 172: 991–998.
51. Preuss, M.L., Serna, J., Falbel, T.G., Bednarek, S.Y., and Nielsen, E. (2004). The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589–1603.
52. Raab, S., Drechsel, G., Zarepour, M., Hartung, W., Koshiba, T., Bittner, F., and Hoth, S. (2009). Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J. 59: 39–51.
53. Robatzek, S., Chinchilla, D., and Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabi-dopsis. Genes Dev. 20: 537–542.
54. Robinson, D.G., Jiang, L., and Schumacher, K. (2008). The endo-somal system of plants: Charting new and familiar territories. Plant Physiol. 147: 1482–1492.
55. Salomon, S., and Robatzek, S. (2006). Induced endocytosis of the receptor kinase FLS2. Plant Signal. Behav. 1: 293–295.
56. Samuel, M.A., Chong, Y.T., Haasen, K.E., Aldea-Brydges, M.G., Stone, S.L., and Goring, D.R. (2009). Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21: 2655–2671.
57. Samuel, M.A., Mudgil, Y., Salt, J.N., Delmas, F., Ramachandran, S., Chilelli, A., and Goring, D.R. (2008). Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol. 147: 2084–2095.
58. Schnatwinkel, C., Christoforidis, S., Lindsay, M.R., Uttenweiler-Joseph, S., Wilm, M., Parton, R.G., and Zerial, M. (2004). The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2: E261.
59. Simonsen, A., Lippé, R., Christoforidis, S., Gaullier, J.-M., Brech, A., Callaghan, J., Toh, B.H., Murphy, C., Zerial, M., and Stenmark, H. (1998). EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494–498.
60. Sparkes, I.A., Runions, J., Kearns, A., and Hawes, C. (2006). Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1: 2019–2025.
61. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10: 513–525.
62. Stenmark, H., Parton, R.G., Steele-Mortimer, O., Lütcke, A., Gruenberg, J., and Zerial, M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13: 1287–1296.
63. Stone, S.L., Anderson, E.M., Mullen, R.T., and Goring, D.R. (2003). ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15: 885–898.
64. Strahl, T., Hama, H., DeWald, D.B., and Thorner, J. (2005). Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus. J. Cell Biol. 171: 967–979.
65. Szumlanski, A.L., and Nielsen, E. (2009). The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21: 526–544.
66. Thole, J.M., and Nielsen, E. (2008). Phosphoinositides in plants: Novel functions in membrane trafficking. Curr. Opin. Plant Biol. 11: 620–631.
67. Trujillo, M., Ichimura, K., Casais, C., and Shirasu, K. (2008). Negative regulation of PAMP-triggered immunity by an E3 ubiquitin li-gase triplet in Arabidopsis. Curr. Biol. 18: 1396–1401.
68. Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A. (2001). Ara6, a plant-unique novel type Rab GTPase, functions in the en-docytic pathway of Arabidopsis thaliana. EMBO J. 20: 4730–4741.
69. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E., and Ryals, J. (1992). Acquired resistance in Arabidopsis. Plant Cell 4: 645–656.
70. van Loon, L.C., and van Strien, E.A. (1999). The families of patho-genesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 554: 85–97.
71. van Loon, L.C., Pierpont, W.S., Boller, T., and Conejero, V. (1994). Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Rep. 12: 245–264.
72. van Loon, L.C., Rep, M., and Pieterse, C.M.J. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44: 135–162.
73. Vega-Sánchez, M.E., Zeng, L., Chen, S., Leung, H., and Wang, G.-L. (2008). SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice. Plant Cell 20: 1456–1469.
74. Vernoud, V., Horton, A.C., Yang, Z., and Nielsen, E. (2003). Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131: 1191–1208.
75. Voigt, B., et al. (2005). Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur. J. Cell Biol. 84: 609–621.
76. Vorwerk, S., Schiff, C., Santamaria, M., Koh, S., Nishimura, M., Vogel, J., Somerville, C., and Somerville, S. (2007). EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol. 7: 35.
77. Walch-Solimena, C., and Novick, P. (1999). The yeast phosphatidylinositol-4-OH kinase pik1 regulates secretion at the Golgi. Nat. Cell Biol. 1: 523–525.
78. Walsh, B.W., Lenhart, J.S., Schroeder, J.W., and Simmons, L.A. (2012). Far western blotting as a rapid and efficient method for detecting interactions between DNA replication and DNA repair proteins. Methods Mol. Biol. 922: 161–168.
79. Wang, Y.J., Wang, J., Sun, H.Q., Martinez, M., Sun, Y.X., Macia, E., Kirchhausen, T., Albanesi, J.P., Roth, M.G., and Yin, H.L. (2003). Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114: 299–310.
80. Yan, J., Wang, J., Li, Q., Hwang, J.R., Patterson, C., and Zhang, H. (2003). AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol. 132: 861–869.
81. Yang, C.-W., González-Lamothe, R., Ewan, R.A., Rowland, O., Yoshioka, H., Shenton, M., Ye, H., O’Donnell, E., Jones, J.D.G., and Sadanandom, A. (2006). The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 18: 1084–1098.
82. Zeng, L.-R., Qu, S., Bordeos, A., Yang, C., Baraoidan, M., Yan, H., Xie, Q., Nahm, B.H., Leung, H., and Wang, G.-L. (2004). Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16: 2795–2808.
83. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2: 107–117.