A Moving View: Subcellular Trafficking Processes in Pattern Recognition ReceptorTriggered Plant Immunity

Annual Review of Phytopathology

Volumn 53, Issue , 2015, Pages 379-402

  Ben Khaled, Sara ^a   Postma, Jelle ^a   Robatzek, Silke ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

Endocytosis; FLS2; MAMP; Membrane trafficking; PRR

Indexed keywords

PATTERN RECOGNITION RECEPTOR; VEGETABLE PROTEIN;

GENETICS; IMMUNOLOGY; METABOLISM; PLANT; PLANT IMMUNITY; PROTEIN TRANSPORT;

PLANT IMMUNITY; PLANT PROTEINS; PLANTS; PROTEIN TRANSPORT; RECEPTORS, PATTERN RECOGNITION;

EID: 84938694398     PISSN: 00664286     EISSN: 15452107     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080614-120347     Document Type: Review

References (156)

1. Ali GS, Prasad KV, Day I, Reddy AS. 2007. Ligand-dependent reduction in the membrane mobility of FLAGELLIN SENSITIVE2, an Arabidopsis receptor-like kinase. Plant Cell Physiol. 48:1601-11
2. An Q, Ehlers K, Kogel KH, van Bel AJ, Huckelhoven R. 2006. Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol. 172:563-76
3. An Q, Huckelhoven R, Kogel KH, van Bel AJ. 2006. Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell. Microbiol. 8:1009-19
4. Asai T, Tena G, Plotnikova J, Willmann M, Chiu W, et al. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-83
5. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, et al. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15:5118-29
6. BarM, Avni A. 2009.EHD2inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J. Cell Mol. Biol. 59:600-11
7. BarM, Avni A. 2009. EHD2 inhibits signaling of leucine rich repeat receptor-like proteins. Plant Signal. Behav. 4:682-84
8. Bar M, Sharfman M, Ron M, Avni A. 2010. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. Cell Mol. Biol. 63:791-800
9. Bar M, Sharfman M, Schuster S, Avni A. 2009. The coiled-coil domain of EHD2 mediates inhibition of LeEix2 endocytosis and signaling. PLOS ONE 4:e7973
10. Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, et al. 2013. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 64:5309-21
11. Bauer Z, Gomez-Gomez L, Boller T, Felix G. 2001. Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J. Biol. Chem. 276:45669-76
12. Beck M, HeardW, Mbengue M, Robatzek S. 2012. The INs and OUTsof pattern recognition receptors at the cell surface. Curr. Opin. Plant Biol. 15:367-74
13. Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A, et al. 2014. Expression patterns of FLAGELLIN SENSING 2 map to bacterial entry sites in plant shoots and roots. J. Exp. Bot. 65:6487-98
14. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. 2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24:4205-19
15. Becsi B, Kiss A, Erdodi F. 2014. Interaction of protein phosphatase inhibitors with membrane lipids assessed by surface plasmon resonance based binding technique. Chem. Phys. Lipids 183:68-76
16. Benschop JJ, Mohammed S, OFlaherty M, Heck AJ, Slijper M, Menke FL. 2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 6:1198-214
17. Bogdanove AJ, Martin GB. 2000. AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc. Natl. Acad. Sci. USA 97:8836-40
18. Bohlenius H, Morch SM, Godfrey D, Nielsen ME, Thordal-Christensen H. 2010. The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 22:3831-44
19. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379-406
20. Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B. 2004. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214:159-73
21. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, et al. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418-22
22. Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH, et al. 2014. Rerouting of plant late endocytic trafficking towards a pathogen interface. Traffic 16:204-26
23. BozkurtTO, Schornack S, Win J, ShindoT, Ilyas M, et al. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl. Acad. Sci. USA 108:20832-37
24. Bucherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH, et al. 2013. Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol. 162:1911-25
25. Caaveiro JM, Molina A, Gonzalez-Manas JM, Rodriguez-Palenzuela P, Garcia-Olmedo F, Goni FM. 1997. Differential effects of five types of antipathogenic plant peptides on model membranes. FEBS Lett. 410:338-42
26. Carmona MJ, Molina A, Fernandez JA, Lopez-Fando JJ, Garcia-Olmedo F. 1993. Expression of the alpha-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens. Plant J. Cell Mol. Biol. 3:457-62
27. Chaparro-Garcia A, Schwizer S, Sklenar J, YoshidaK, Bos JIB, et al. 2014. Phytophthora infestans RXLRWYeffector AVR3a associates with a dynamin-related protein involved in endocytosis of a plant pattern recognition receptor. Cold Spring Harb. Lab. doi: http://dx.doi.org/10.1101/012963
28. Chen L, Hamada S, Fujiwara M, Zhu T, Thao NP, et al. 2010. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7:185-96
29. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. 2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465-76
30. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497-500
31. Choi SW, Tamaki T, Ebine K, Uemura T, Ueda T, Nakano A. 2013. RABA members act in distinct steps of subcellular trafficking of the FLAGELLIN SENSING2 receptor. Plant Cell 25:1174-87
32. Collings DA, Gebbie LK, Howles PA, Hurley UA, Birch RJ, et al. 2008. Arabidopsis dynamin-like protein DRP1A: A null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion. J. Exp. Bot. 59:361-76
33. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, et al. 2003. SNARE-proteinmediated disease resistance at the plant cell wall. Nature 425:973-77
34. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA 109:5110-15
35. Delmotte N, KniefC, Chaffron S, Innerebner G, Roschitzki B, et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA 106:16428-33
36. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, et al. 2007. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17:520-27
37. Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, et al. 2012. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 22:413-24
38. Du Y. 2014. Phytophthora infestans RXLR effector AVR1 and its host target Sec5. PhD Thesis, Wageningen Univ., Wageningen, Neth
39. Du Y, Tejos R, BeckM, Himschoot E, Li H, et al. 2013. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc. Natl. Acad. Sci. USA 110:7946-51
40. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, et al. 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. USA 110:8744-49
41. Eitas TK, Dangl JL. 2010. NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13:472-77
42. Emans N, Zimmermann S, Fischer R. 2002. Uptake of a fluorescent marker in plant cells is sensitive to Brefeldin A andWortmannin. Plant Cell 14:71-86
43. Epel BL. 1994. Plasmodesmata: composition, structure and trafficking. Plant Mol. Biol. 26:1343-56
44. Farid A, Malinovsky FG, Veit C, Schoberer J, Zipfel C, Strasser R. 2013. Specialized roles of the conserved subunit OST3/6 of the oligosaccharyltransferase complex in innate immunity and tolerance to abiotic stresses. Plant Physiol. 162:24-38
45. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, et al. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl. Acad. Sci. USA 110:9166-70
46. Faulkner C, Robatzek S. 2012. Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr. Opin. Plant Biol. 15:699-707
47. Felix G, Duran J, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-76
48. Fujimoto M, Arimura S-I, Ueda T, Takanashi H, Hayashi Y, et al. 2010. Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc. Natl. Acad. Sci. USA 107:6094-99
49. Fujimoto M, Arimura S, Nakazono M, Tsutsumi N. 2008. Arabidopsis dynamin-related protein DRP2B is co-localized with DRP1A on the leading edge of the forming cell plate. Plant Cell Rep. 27:1581-86
50. Gao X, Guo Y. 2012. CLE peptides in plants: proteolytic processing, structure-activity relationship, and ligand-receptor interaction. J. Integr. Plant Biol. 54:738-45
51. Gaspar YM, McKenna JA, McGinness BS, Hinch J, Poon S, et al. 2014. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J. Exp. Bot. 65:1541-50
52. Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824-32
53. Gomez-Gomez L, Boller T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-11
54. Gomez-Gomez L, Felix G, Boller T. 1999. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 18:277-84
55. Grebe M, Xu J, Möbius W, Ueda T, Nakano A, et al. 2003. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13:1378-87
56. Gu Y, Innes RW. 2012. The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24:4717-30
57. Haglund K, Fiore PD, Dikic I. 2003. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28:598-603
58. Hann DR, Rathjen JP. 2007. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. Cell Mol. Biol. 49:607-18
59. Hao H, Fan L, Chen T, Li R, Li X, et al. 2014. Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26:1729-45
60. Haweker H, Rips S, Koiwa H, Salomon S, Saijo Y, et al. 2010. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285:4629-36
61. Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ. 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLOS Pathog. 9:e1003290
62. Hicke L, Dunn R. 2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19:141-72
63. Honkanen RE. 1993. Cantharidin, another natural toxin that inhibits the activity of serine/threonine protein phosphatases types 1 and 2A. FEBS Lett. 330:283-86
64. Huang J, FujimotoM, FujiwaraM, Fukao Y, Arimura S, TsutsumiN. 2015. Arabidopsis dynamin-related proteins, DRP2A and DRP2B, function coordinately in post-Golgi trafficking. Biochem. Biophys. Res. Commun. 456:238-44
65. Huss M, IngenhorstG, Konig S, GasselM, Drose S, et al. 2002. Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J. Biol. Chem. 277:40544-48
66. Irani NG, Di Rubbo S, Mylle E, Van Den Begin J, Schneider-Pizon J, et al. 2012. Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat. Chem. Biol. 8:583-89
67. Jarsch IK, Konrad SS, Stratil TF, Urbanus SL, SzymanskiW, et al. 2014. Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698-711
68. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43-55
69. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 103:11086-91
70. Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW, et al. 2014. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLOS Pathog. 10(6):e1004232
71. KeinathNF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, et al. 2010.PAMP(pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285:39140-49
72. Kim BH, Kim SY, Nam KH. 2013. Assessing the diverse functions of BAK1 and its homologs in Arabidopsis, beyond BR signaling and PTI responses. Mol. Cells 35:7-16
73. Korasick DA, McMichael C, Walker KA, Anderson JC, Bednarek SY, Heese A. 2010. Novel functions of stomatal cytokinesis-defective 1 (SCD1) in innate immune responses against bacteria. J. Biol. Chem. 285:23342-50
74. Kwaaitaal MA, de Vries SC, Russinova E. 2005. Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 226:55-65
75. Lee AHY, Hurley B, Felsensteiner C, Yea C. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLOS Pathog. 9(2):e1002523
76. Lee H, Khatri A, Plotnikov JM, Zhang XC, Sheen J. 2012. Complexity in differential peptide-receptor signaling: response to Segonzac et al. And Mueller et al. Commentaries. Plant Cell 24:3177-85
77. Lee HY, Bowen CH, Popescu GV, Kang HG, Kato N, et al. 2011. Arabidopsis RTNLB1 and RTNLB2 reticulon-like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell 23:3374-91
78. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ. 2010. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137:467-76
79. Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M, et al. 2009. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl. Acad. Sci. USA 106:15973-78
80. Li W, Ahn IP, Ning Y, Park CH, Zeng L, et al. 2012. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol. 159:239-50
81. Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, et al. 2013. Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384-87
82. Liebrand TW, Kombrink A, Zhang Z, Sklenar J, Jones AM, et al. 2014. Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium. Mol. Plant Pathol. 15:109-17
83. Liebrand TW, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JH, et al. 2012. Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol. 159:1819-33
84. Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH, et al. 2013. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. USA 110:10010-15
85. Lu D, LinW, Gao X, WuS, Cheng C, et al. 2011. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439-42
86. Lu X, Tintor N, Mentzel T, Kombrink E, Boller T, et al. 2009. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl. Acad. Sci. USA 106:22522-27
87. Lu YJ, Schornack S, SpallekT, Geldner N, Chory J, et al. 2012. Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell. Microbiol. 14:682-97
88. Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C, et al. 2014. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343:1509-12
89. Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54:263-72
90. Macnab RM. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100
91. Malinovsky FG, Brodersen P, Fiil BK, McKinney LV, Thorgrimsen S, et al. 2010. Lazarus1, a DUF300 protein, contributes to programmed cell death associated with Arabidopsis acd11 and the hypersensitive response. PLOS ONE 5:e12586
92. McMichael CM, Reynolds GD, Koch LM, Wang C, Jiang N, et al. 2013. Mediation of clathrindependent trafficking during cytokinesis and cell expansion by Arabidopsis stomatal cytokinesis defective proteins. Plant Cell 25:3910-25
93. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969-80
94. Meyer D, Pajonk S, Micali C, OConnell R, Schulze-Lefert P. 2009. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. Cell Mol. Biol. 57:986-99
95. Micali CO, Neumann U, Grunewald D, Panstruga R, OConnell R. 2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell Microbiol. 13:210-26
96. MishinaTE, Zeier J. 2007. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. Cell Mol. Biol. 50:500-13
97. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:19613-18
98. Morel JB, Dangl JL. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4:671-83
99. Mukhtar MS, Carvunis A-RR, Dreze M, Epple P, Steinbrenner J, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596-601
100. Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, et al. 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28:3428-38
101. Nielsen ME, Feechan A, Bohlenius H, Ueda T, Thordal-Christensen H. 2012. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc. Natl. Acad. Sci. USA 109:11443-48
102. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY. 2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220-23
103. Nomura K, Mecey C, Lee Y-NN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc. Natl. Acad. Sci. USA 108:10774-79
104. Ntoukakis V, Schwessinger B, Segonzac C, Zipfel C. 2011. Cautionary notes on the use of C-terminal BAK1 fusion proteins for functional studies. Plant Cell 23:3871-78
105. OConnell RJ, Panstruga R. 2006. Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171:699-718
106. Ohno H, Fournier MC, Poy G, Bonifacino JS. 1996. Structural determinants of interaction of tyrosinebased sorting signals with the adaptor medium chains. J. Biol. Chem. 271:29009-15
107. Park CJ, Bart R, Chern M, Canlas PE, Bai W, Ronald PC. 2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLOS ONE 5:e9262
108. Peer WA, Hosein FN, Bandyopadhyay A, Makam SN, Otegui MS, et al. 2009. Mutation of the membrane-associated M1 protease APM1 results in distinct embryonic and seedling developmental defects in Arabidopsis. Plant Cell 21:1693-721
109. Perez-Gomez J, Moore I. 2007. Plant endocytosis: It is clathrin after all. Curr. Biol. 17:R217-19
110. Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, et al. 2015. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. In press
111. Richter S, Kientz M, Brumm S, Nielsen ME, Park M, et al. 2014. Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. Elife 3:e02131
112. Robatzek S, Chinchilla D, Boller T. 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20:537-42
113. Romeis T, Ludwig A, Martin R, Jones J. 2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20:5556-67
114. RonM, Avni A. 2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604-15
115. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB. 2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370-74
116. Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, et al. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216-29
117. Salomon S, Robatzek S. 2006. Induced endocytosis of the receptor kinase FLS2. Plant Signal. Behav. 6:293-95
118. Scheuring D, Viotti C, Kruger F, Kunzl F, Sturm S, et al. 2011. Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23:3463-81
119. Schmidt O, Teis D. 2012. The ESCRT machinery. Curr. Biol. 22:R116-20
120. Schmidt SM, Kuhn H, Micali C, Liller C, Kwaaitaal M, Panstruga R. 2014. Interaction of a Blumeria graminis f. Sp. Hordei effector candidate with a barley ARF-GAP suggests that host vesicle trafficking is a fungal pathogenicity target. Mol. Plant Pathol. 15:535-49
121. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, et al. 2010. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285:9444-51
122. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, et al. 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLOS Genet. 7:e1002046
123. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, Rathjen JP. 2011. Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol. 156:687-99
124. Serrano M, Robatzek S, Torres M, Kombrink E, Somssich IE, et al. 2007. Chemical interference of pathogen-associated molecular pattern-triggered immune responses in Arabidopsis reveals a potential role for fatty-acid synthase type II complex-derived lipid signals. J. Biol. Chem. 282:6803-11
125. Sharfman M, Bar M, Ehrlich M, Schuster S, Melech-Bonfil S, et al. 2011. Endosomal signaling of the tomato leucine-rich repeat receptor-like protein LeEix2. Plant J. Cell Mol. Biol. 68:413-23
126. SharfmanM, Bar M, Schuster S, LeibmanM, Avni A. 2014. Sterol-dependent induction of plant defense responses by a microbe-associated molecular pattern from Trichoderma viride. Plant Physiol. 164:819-27
127. Smith JM, Leslie ME, Robinson SJ, Korasick DA, Zhang T, et al. 2014. Loss of Arabidopsis thaliana dynamin-related protein 2B reveals separation of innate immune signaling pathways. PLOS Pathog. 10:e1004578
128. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-6
129. Spallek T, Beck M, Ben Khaled S, Salomon S, Bourdais G, et al. 2013. ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLOS Genet. 9:e1004035
130. Spallek T, Robatzek S, Gohre V. 2009. How microbes utilize host ubiquitination. Cell. Microbiol. 11:1425-34
131. Sparkes I, TolleyN, Aller I, Svozil J, Osterrieder A, et al. 2010. Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 22:1333-43
132. Speth EB, Imboden L, Hauck P, He SY. 2009. Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol. 149:1824-37
133. Stegmann M, Anderson RG, Ichimura K, Pecenkova T, Reuter P, et al. 2012. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24:4703-16
134. StotzHU, Mitrousia GK, deWit PJ, Fitt BD. 2014. Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci. 19:491-500
135. SunT, Zhang Q, GaoM, Zhang Y. 2014. Regulation of SOBIR1 accumulation and activation of defense responses in bir1-1 by specific components of ER quality control. Plant J. Cell Mol. Biol. 77:748-56
136. Sun Y, Li L, Macho AP, Han Z, Hu Z, et al. 2013. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624-28
137. Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J. 2009. Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr. Biol. 19:391-97
138. Tateda C, Zhang Z, Shrestha J, Jelenska J, Chinchilla D, Greenberg JT. 2014. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26:4171-87
139. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, et al. 1997. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209-24
140. Tilsner J, Amari K, Torrance L. 2011. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39-60
141. Tintor N, Ross A, Kanehara K, Yamada K, Fan L, et al. 2013. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. USA 110:6211-16
142. Toth R, Gerding-Reimers C, DeeksMJ, Menninger S, Gallegos RM, et al. 2012. Prieurianin/endosidin 1 is an actin-stabilizing small molecule identified from a chemical genetic screen for circadian clock effectors in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 71:338-52
143. Trujillo M, Ichimura K, Casais C, Shirasu K. 2008. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18:1396-401
144. Underwood W, Somerville SC. 2008. Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59:3501-8
145. Underwood W, Somerville SC. 2013. Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. Proc. Natl. Acad. Sci. USA 110:12492-97
146. Wang D, Weaver ND, Kesarwani M, Dong X. 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036-40
147. Wang J, Cai Y, Miao Y, Lam SK, Jiang L. 2009. Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60:3075-83
148. Weßling R, Epple P, Altmann S, He Y, Yang L, et al. 2014. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364-75
149. Xin XF, Nomura K, Underwood W, He SY. 2013. Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv. tomato DC3000 infection of Arabidopsis. Mol. Plant-Microbe Interact. 26:861-67
150. Yun HS, Kwaaitaal M, Kato N, Yi C, Park S, et al. 2013. Requirement of vesicle-associated membrane protein 721 and 722 for sustained growth during immune responses in Arabidopsis. Mol. Cells 35:481-88
151. Zeng W, He SY. 2010. A prominent role of the flagellin receptor FLAGELLIN-SENSING2 inmediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol. 153:1188-98
152. Zhang Z, Lenk A, AnderssonMX, Gjetting T, Pedersen C, et al. 2008. A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol. Plant 1:510-27
153. Zhang Z, Shrestha J, Tateda C, Greenberg JT. 2014. Salicylic acid signaling controls the maturation and localization of the Arabidopsis defense protein ACCELERATED CELL DEATH6. Mol. Plant 7:1365-83
154. Zhao T, Rui L, Li J, Nishimura M, Vogel J, et al. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLOS Genet. 11:e1004945
155. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749-60
156. Zipfel C, Robatzek S. 2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi. .? Plant Physiol. 154:551-54