Endosomal trafficking and signaling in plant defense responses

Current Opinion in Plant Biology

Volumn 22, Issue , 2014, Pages 86-92

  Bar, Maya ^a   Avni, Adi ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE; ENDOSOME; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

CELL MEMBRANE; ENDOSOMES; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84907533737     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.09.008     Document Type: Review

References (70)

1. Thomma B.P.H.J., Nurnberger T., Joosten M.H.A.J. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 2011, 23:4-15.
2. Geldner N., Robatzek S. Plant receptors go endosomal: a moving view on signal transduction. Plant Physiol 2008, 147:1565-1574.
3. Robatzek S. Vesicle trafficking in plant immune responses. Cell Microbiol 2007, 9:1-8.
4. Elbaz M., Avni A., Weil M. Constitutive caspase-like machinery executes programmed cell death in plant cells. Cell Death Differ 2002, 9:726-733.
5. Henry G., Thonart P., Ongena M. PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biotechnol Agron Soc Environ 2012, 16:257-268.
6. Chinchilla D., Boller T. Innate immunity pattern recognition in plants. Effectors in plant-microbe interactions 2011, 3-34. Wiley-Blackwell. F. Martin, S. Kamoun (Eds.).
7. Patel H.H., Murray F., Insel P.A. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 2008, 48:359-391.
8. Bar M., Avni A. EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J 2009, 59:600-611.
9. Leborgne-Castel N., Lherminier J., Der C., Fromentin J., Houot V., Simon-Plas F. The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in Bright Yellow-2 tobacco cells. Plant Physiol 2008, 146:1255-1266.
10. Robatzek S., Chinchilla D., Boller T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 2006, 20:537-542.
11. Sharfman M., Bar M., Ehrlich M., Schuster S., Melech-Bonfil S., Ezer R., Sessa G., Avni A. Endosomal signaling of the tomato leucine-rich repeat receptor-like protein LeEix2. Plant J 2011, 68:413-423.
12. Bohm H., Albert I., Fan L., Reinhard A., Nurnberger T. Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 2014, 20C:47-54.
13. Lee M.S., Min Y.J. Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 2007, 76:447-480.
14. Kobe B., Kajava A.V. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 2001, 11:725-732.
15. Sun Y., Li L., Macho A.P., Han Z., Hu Z., Zipfel C., Zhou J.M., Chai J. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 2013, 342:624-628.
16. Wulff B.B., Heese A., Tomlinson-Buhot L., Jones D.A., de la Pena M., Jones J.D. The major specificity-determining amino acids of the tomato Cf-9 disease resistance protein are at hypervariable solvent-exposed positions in the central leucine-rich repeats. Mol Plant Microbe Interact 2009, 22:1203-1213.
17. Parniske M., Hammond-Kosack K.E., Golstein C., Thomas C.M., Jones D.A., Harrison K., Wulff B.B., Jones J.D. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 1997, 91:821-832.
18. Fradin E.F., Zhang Z., Rovenich H., Song Y., Liebrand T.W.H., Masini L., van den Berg G.C.M., Joosten M.H.A.J., Thomma B.P.H.J. Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2. PLOS ONE 2014, 9.
19. Zhang Z., Song Y., Liu C.M., Thomma B.P. Mutational analysis of the ve1 immune receptor that mediates verticillium resistance in tomato. PLOS ONE 2014, 9:e99511.
20. Ron M., Avni A. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 2004, 16:1604-1615.
21. Beck M., Bourdais G., Kopischke M., Mbengue M., Postma J., Spallek T., Liebrand T., Joosten M., Robatzek S. Traffic control for receptors at the host-microbe interface. XVI-IS-MPMI 2014, Greece, Rhodes.
22. Kozik P., Francis R.W., Seaman M.N., Robinson M.S. A screen for endocytic motifs. Traffic 2010, 11:843-855.
23. Beck M., Heard W., Mbengue M., Robatzek S. The INs and OUTs of pattern recognition receptors at the cell surface. Curr Opin Plant Biol 2012, 15:367-374.
24. Beck M., Zhou J., Faulkner C., MacLean D., Robatzek S. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 2012, 24:4205-4219.
25. Liebrand T.W.H., van den Burg H.A., Joosten M.H.A.J. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 2014, 19:123-132.
26. Liebrand T.W.H., van den Berg G.C.M., Zhang Z., Smit P., Cordewener J.H.G., America A.H.P., Sklenar J., Jones A.M.E., Tameling W.I.L., Robatzek S., et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci U S A 2013, 110:10010-10015.
27. Chinchilla D., Zipfel C., Robatzek S., Kemmerling B., Nurnberger T., Jones J.D., Felix G., Boller T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007, 448:497-500.
28. Heese A., Hann D.R., Gimenez-Ibanez S., Jones A.M., He K., Li J., Schroeder J.I., Peck S.C., Rathjen J.P. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 2007, 104:12217-12222.
29. Schulze B., Mentzel T., Jehle A.K., Mueller K., Beeler S., Boller T., Felix G., Chinchilla D. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 2010, 285:9444-9451.
30. Bar M., Sharfman M., Ron M., Avni A. BAK1 is required for the attenuation of Eix-induced defense responses by the decoy receptor LeEix1. Plant J 2010, 63:791-800.
31. Fradin E.F., Zhang Z., Juarez Ayala J.C., Castroverde C.D., Nazar R.N., Robb J., Liu C.M., Thomma B.P. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 2009, 150:320-332.
32. Fradin E.F., Abd-El-Haliem A., Masini L., van den Berg G.C., Joosten M.H., Thomma B.P. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol 2011, 156:2255-2265.
33. Bar M., Avni A. EHD2 inhibits signaling of leucine rich repeat receptor-like proteins. Plant Signal Behav 2009, 4:682-684.
34. Hansen C.G., Nichols B.J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 2010, 20:177-186.
35. Bargmann B.O., Laxalt A.M., Riet B.T., Schouten E., van Leeuwen W., Dekker H.L., de Koster C.G., Haring M.A., Munnik T. LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J 2006, 45:358-368.
36. Laxalt A.M., ter Riet B., Verdonk J.C., Parigi L., Tameling W.I., Vossen J., Haring M., Musgrave A., Munnik T. Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. Plant J 2001, 26:237-247.
37. Gonorazky G., Laxalt A.M., Testerink C., Munnik T., de la Canal L. Phosphatidylinositol 4-phosphate accumulates extracellularly upon xylanase treatment in tomato cell suspensions. Plant Cell Environ 2008, 31:1051-1062.
38. Golani Y., Kaye Y., Gilhar O., Ercetin M., Gillaspy G., Levine A. Inositol polyphosphate phosphatidylinositol 5-phosphatase9 (At5ptase9) controls plant salt tolerance by regulating endocytosis. Mol Plant 2013, 6:1781-1794.
39. Sharfman M., Bar M., Schuster S., Leibman M., Avni A. Sterol-dependent induction of plant defense responses by a microbe-associated molecular pattern from Trichoderma viride. Plant Physiol 2014, 164:819-827.
40. Bar M., Sharfman M., Schuster S., Avni A. The coiled-coil domain of EHD2 mediates inhibition of LeEix2 endocytosis and signaling. PLoS ONE 2009, 4:e7973.
41. Adam T., Bouhidel K., Der C., Robert F., Najid A., Simon-Plas F., Leborgne-Castel N. Constitutive expression of clathrin hub hinders elicitor-induced clathrin-mediated endocytosis and defense gene expression in plant cells. FEBS Lett 2012, 586:3293-3298.
42. Hayakawa A., Hayes S.J., Lawe D.C., Sudharshan E., Tuft R., Fogarty K., Lambright D., Corvera S. Structural basis for endosomal targeting by FYVE domains. J Biol Chem 2004, 279:5958-5966.
43. Baisa G.A., Mayers J.R., Bednarek S.Y. Budding and braking news about clathrin-mediated endocytosis. Curr Opin Plant Biol 2013, 16:718-725.
44. Lipka V., Panstruga R. Dynamic cellular responses in plant-microbe interactions. Curr Opin Plant Biol 2005, 8:625-631.
45. Schmelzer E. Cell polarization, a crucial process in fungal defence. Trends Plant Sci 2002, 7:411-415.
46. Henty-Ridilla J.L., Shimono M., Li J., Chang J.H., Day B., Staiger C.J. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLOS Pathog 2013, 9:e1003290.
47. Smith J.M., Salamango D.J., Leslie M.E., Collins C.A., Heese A. Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol 2014, 164:440-454.
48. Spallek T., Beck M., Ben Khaled S., Salomon S., Bourdais G., Schellmann S., Robatzek S. ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLOS Genet 2013, 9.
49. Rajagopalan S. Endosomal signaling and a novel pathway defined by the natural killer receptor KIR2DL4 (CD158d). Traffic 2010, 11:1381-1390.
50. Diguglielmo G.M., Baass P.C., Ou W.J., Posner B.I., Bergeron J.J.M. Compartmentalization of Shc, Grb2 and Msos, and hyperphosphorylation of Raf-1 by Egf but not insulin in liver parenchyma. EMBO J 1994, 13:4269-4277.
51. Baass P.C., Diguglielmo G.M., Authier F., Posner B.I., Bergeron J.J.M. Compartmentalized signal-transduction by receptor tyrosine kinases. Trends Cell Biol 1995, 5:465-470.
52. Murphy J.E., Padilla B.E., Hasdemir B., Cottrell G.S., Bunnett N.W. Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci U S A 2009, 106:17615-17622.
53. Geldner N., Hyman D.L., Wang X., Schumacher K., Chory J. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 2007, 21:1598-1602.
54. Irani N.G., Di Rubbo S., Mylle E., Van den Begin J., Schneider-Pizon J., Hnilikova J., Sisa M., Buyst D., Vilarrasa-Blasi J., Szatmari A.M., et al. Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat Chem Biol 2012, 8:583-589.
55. Drakakaki G., van de Ven W., Pan S., Miao Y., Wang J., Keinath N.F., Weatherly B., Jiang L., Schumacher K., Hicks G., et al. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res 2012, 22:413-424.
56. Geldner N., Denervaud-Tendon V., Hyman D.L., Mayer U., Stierhof Y.D., Chory J. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 2009, 59:169-178.
57. Contento A.L., Bassham D.C. Structure and function of endosomes in plant cells. J Cell Sci 2012, 125:3511-3518.
58. Bolte S., Talbot C., Boutte Y., Catrice O., Read N.D., Satiat-Jeunemaitre B. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 2004, 214:159-173.
59. Naramoto S., Otegui M.S., Kutsuna N., de Rycke R., Dainobu T., Karampelias M., Fujimoto M., Feraru E., Miki D., Fukuda H., et al. Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell 2014, 26:3062-3076.
60. Viotti C., Bubeck J., Stierhof Y.D., Krebs M., Langhans M., van den Berg W., van Dongen W., Richter S., Geldner N., Takano J., et al. Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 2010, 22:1344-1357.
61. Tse Y.C., Mo B., Hillmer S., Zhao M., Lo S.W., Robinson D.G., Jiang L. Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 2004, 16:672-693.
62. Bottanelli F., Foresti O., Hanton S., Denecke J. Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 2011, 23:3007-3025.
63. Jaillais Y., Fobis-Loisy I., Miege C., Gaude T. Evidence for a sorting endosome in Arabidopsis root cells. Plant J 2008, 53:237-247.
64. Miao Y., Li K.Y., Li H.Y., Yao X., Jiang L. The vacuolar transport of aleurain-GFP and 2S albumin-GFP fusions is mediated by the same pre-vacuolar compartments in tobacco BY-2 and Arabidopsis suspension cultured cells. Plant J 2008, 56:824-839.
65. Mo B., Tse Y.C., Jiang L. Plant prevacuolar/endosomal compartments. Int Rev Cytol 2006, 253:95-129.
66. Ebine K., Fujimoto M., Okatani Y., Nishiyama T., Goh T., Ito E., Dainobu T., Nishitani A., Uemura T., Sato M.H., et al. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 2011, 13:853-859.
67. Ueda T., Yamaguchi M., Uchimiya H., Nakano A. Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 2001, 20:4730-4741.
68. Henne W.M., Buchkovich N.J., Emr S.D. The ESCRT pathway. Dev Cell 2011, 21:77-91.
69. Scheuring D., Viotti C., Kruger F., Kunzl F., Sturm S., Bubeck J., Hillmer S., Frigerio L., Robinson D.G., Pimpl P., et al. Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 2011, 23:3463-3481.
70. Shahriari M., Richter K., Keshavaiah C., Sabovljevic A., Huelskamp M., Schellmann S. The Arabidopsis ESCRT protein-protein interaction network. Plant Mol Biol 2011, 76:85-96.