1932

Abstract

A significant challenge for plants is to induce localized defense responses at sites of pathogen attack. Therefore, host subcellular trafficking processes enable accumulation and exchange of defense compounds, which contributes to the plant on-site defenses in response to pathogen perception. This review summarizes our current understanding of the transport processes that facilitate immunity, the significance of which is highlighted by pathogens reprogramming membrane trafficking through host cell translocated effectors. Prominent immune-related cargos of plant trafficking pathways are the pattern recognition receptors (PRRs), which must be present at the plasma membrane to sense microbes in the apoplast. We focus on the dynamic localization of the FLS2 receptor and discuss the pathways that regulate receptor transport within the cell and their link to FLS2-mediated immunity. One emerging theme is that ligand-induced late endocytic trafficking is conserved across different PRR protein families as well as across different plant species.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080614-120347
2015-08-04
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/phyto/53/1/annurev-phyto-080614-120347.html?itemId=/content/journals/10.1146/annurev-phyto-080614-120347&mimeType=html&fmt=ahah

Literature Cited

  1. Ali GS, Prasad KV, Day I, Reddy AS. 1.  2007. Ligand-dependent reduction in the membrane mobility of FLAGELLIN SENSITIVE2, an Arabidopsis receptor-like kinase. Plant Cell Physiol. 48:1601–11 [Google Scholar]
  2. An Q, Ehlers K, Kogel KH, van Bel AJ, Huckelhoven R. 2.  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 [Google Scholar]
  3. An Q, Huckelhoven R, Kogel KH, van Bel AJ. 3.  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 [Google Scholar]
  4. Asai T, Tena G, Plotnikova J, Willmann M, Chiu W. 4.  et al. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–83 [Google Scholar]
  5. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L. 5.  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 [Google Scholar]
  6. Bar M, Avni A. 6.  2009. EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J. Cell Mol. Biol. 59:600–11 [Google Scholar]
  7. Bar M, Avni A. 7.  2009. EHD2 inhibits signaling of leucine rich repeat receptor-like proteins. Plant Signal. Behav. 4:682–84 [Google Scholar]
  8. Bar M, Sharfman M, Ron M, Avni A. 8.  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 [Google Scholar]
  9. Bar M, Sharfman M, Schuster S, Avni A. 9.  2009. The coiled-coil domain of EHD2 mediates inhibition of LeEix2 endocytosis and signaling. PLOS ONE 4:e7973 [Google Scholar]
  10. Bartels S, Lori M, Mbengue M, van Verk M, Klauser D. 10.  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 [Google Scholar]
  11. Bauer Z, Gomez-Gomez L, Boller T, Felix G. 11.  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 [Google Scholar]
  12. Beck M, Heard W, Mbengue M, Robatzek S. 12.  2012. The INs and OUTs of pattern recognition receptors at the cell surface. Curr. Opin. Plant Biol. 15:367–74 [Google Scholar]
  13. Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A. 13.  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 [Google Scholar]
  14. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. 14.  2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24:4205–19 [Google Scholar]
  15. Becsi B, Kiss A, Erdodi F. 15.  2014. Interaction of protein phosphatase inhibitors with membrane lipids assessed by surface plasmon resonance based binding technique. Chem. Phys. Lipids 183:68–76 [Google Scholar]
  16. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJ, Slijper M, Menke FL. 16.  2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 6:1198–214 [Google Scholar]
  17. Bogdanove AJ, Martin GB. 17.  2000. AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc. Natl. Acad. Sci. USA 97:8836–40 [Google Scholar]
  18. Bohlenius H, Morch SM, Godfrey D, Nielsen ME, Thordal-Christensen H. 18.  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 [Google Scholar]
  19. Boller T, Felix G. 19.  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 [Google Scholar]
  20. Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B. 20.  2004. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214:159–73 [Google Scholar]
  21. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L. 21.  et al. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–22 [Google Scholar]
  22. Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH. 22.  et al. 2014. Rerouting of plant late endocytic trafficking towards a pathogen interface. Traffic 16:204–26 [Google Scholar]
  23. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M. 23.  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 [Google Scholar]
  24. Bucherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH. 24.  et al. 2013. Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol. 162:1911–25 [Google Scholar]
  25. Caaveiro JM, Molina A, Gonzalez-Manas JM, Rodriguez-Palenzuela P, Garcia-Olmedo F, Goni FM. 25.  1997. Differential effects of five types of antipathogenic plant peptides on model membranes. FEBS Lett. 410:338–42 [Google Scholar]
  26. Carmona MJ, Molina A, Fernandez JA, Lopez-Fando JJ, Garcia-Olmedo F. 26.  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 [Google Scholar]
  27. Chaparro-Garcia A, Schwizer S, Sklenar J, Yoshida K, Bos JIB. 27.  et al. 2014. Phytophthora infestans RXLR-WY effector 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 [Google Scholar]
  28. Chen L, Hamada S, Fujiwara M, Zhu T, Thao NP. 28.  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 [Google Scholar]
  29. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. 29.  2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–76 [Google Scholar]
  30. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T. 30.  et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500 [Google Scholar]
  31. Choi SW, Tamaki T, Ebine K, Uemura T, Ueda T, Nakano A. 31.  2013. RABA members act in distinct steps of subcellular trafficking of the FLAGELLIN SENSING2 receptor. Plant Cell 25:1174–87 [Google Scholar]
  32. Collings DA, Gebbie LK, Howles PA, Hurley UA, Birch RJ. 32.  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 [Google Scholar]
  33. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E. 33.  et al. 2003. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–77 [Google Scholar]
  34. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P. 34.  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 [Google Scholar]
  35. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B. 35.  et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA 106:16428–33 [Google Scholar]
  36. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J. 36.  et al. 2007. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17:520–27 [Google Scholar]
  37. Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J. 37.  et al. 2012. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 22:413–24 [Google Scholar]
  38. Du Y. 38.  2014. Phytophthora infestans RXLR effector AVR1 and its host target Sec5. PhD Thesis, Wageningen Univ., Wageningen, Neth. [Google Scholar]
  39. Du Y, Tejos R, Beck M, Himschoot E, Li H. 39.  et al. 2013. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc. Natl. Acad. Sci. USA 110:7946–51 [Google Scholar]
  40. Dubiella U, Seybold H, Durian G, Komander E, Lassig R. 40.  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 [Google Scholar]
  41. Eitas TK, Dangl JL. 41.  2010. NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13:472–77 [Google Scholar]
  42. Emans N, Zimmermann S, Fischer R. 42.  2002. Uptake of a fluorescent marker in plant cells is sensitive to Brefeldin A and Wortmannin. Plant Cell 14:71–86 [Google Scholar]
  43. Epel BL. 43.  1994. Plasmodesmata: composition, structure and trafficking. Plant Mol. Biol. 26:1343–56 [Google Scholar]
  44. Farid A, Malinovsky FG, Veit C, Schoberer J, Zipfel C, Strasser R. 44.  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 [Google Scholar]
  45. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S. 45.  et al. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl. Acad. Sci. USA 110:9166–70 [Google Scholar]
  46. Faulkner C, Robatzek S. 46.  2012. Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr. Opin. Plant Biol. 15:699–707 [Google Scholar]
  47. Felix G, Duran J, Volko S, Boller T. 47.  1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265–76 [Google Scholar]
  48. Fujimoto M, Arimura S-I, Ueda T, Takanashi H, Hayashi Y. 48.  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 [Google Scholar]
  49. Fujimoto M, Arimura S, Nakazono M, Tsutsumi N. 49.  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 [Google Scholar]
  50. Gao X, Guo Y. 50.  2012. CLE peptides in plants: proteolytic processing, structure-activity relationship, and ligand-receptor interaction. J. Integr. Plant Biol. 54:738–45 [Google Scholar]
  51. Gaspar YM, McKenna JA, McGinness BS, Hinch J, Poon S. 51.  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 [Google Scholar]
  52. Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T. 52.  et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824–32 [Google Scholar]
  53. Gomez-Gomez L, Boller T. 53.  2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003–11 [Google Scholar]
  54. Gomez-Gomez L, Felix G, Boller T. 54.  1999. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 18:277–84 [Google Scholar]
  55. Grebe M, Xu J, Möbius W, Ueda T, Nakano A. 55.  et al. 2003. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13:1378–87 [Google Scholar]
  56. Gu Y, Innes RW. 56.  2012. The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24:4717–30 [Google Scholar]
  57. Haglund K, Fiore PD, Dikic I. 57.  2003. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28:598–603 [Google Scholar]
  58. Hann DR, Rathjen JP. 58.  2007. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. Cell Mol. Biol. 49:607–18 [Google Scholar]
  59. Hao H, Fan L, Chen T, Li R, Li X. 59.  et al. 2014. Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26:1729–45 [Google Scholar]
  60. Haweker H, Rips S, Koiwa H, Salomon S, Saijo Y. 60.  et al. 2010. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285:4629–36 [Google Scholar]
  61. Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ. 61.  2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLOS Pathog. 9:e1003290 [Google Scholar]
  62. Hicke L, Dunn R. 62.  2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19:141–72 [Google Scholar]
  63. Honkanen RE. 63.  1993. Cantharidin, another natural toxin that inhibits the activity of serine/threonine protein phosphatases types 1 and 2A. FEBS Lett. 330:283–86 [Google Scholar]
  64. Huang J, Fujimoto M, Fujiwara M, Fukao Y, Arimura S, Tsutsumi N. 64.  2015. Arabidopsis dynamin-related proteins, DRP2A and DRP2B, function coordinately in post-Golgi trafficking. Biochem. Biophys. Res. Commun. 456:238–44 [Google Scholar]
  65. Huss M, Ingenhorst G, Konig S, Gassel M, Drose S. 65.  et al. 2002. Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J. Biol. Chem. 277:40544–48 [Google Scholar]
  66. Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider-Pizon J. 66.  et al. 2012. Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat. Chem. Biol. 8:583–89 [Google Scholar]
  67. Jarsch IK, Konrad SS, Stratil TF, Urbanus SL, Szymanski W. 67.  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 [Google Scholar]
  68. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S. 68.  et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55 [Google Scholar]
  69. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. 69.  et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 103:11086–91 [Google Scholar]
  70. Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW. 70.  et al. 2014. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLOS Pathog. 10:6e1004232 [Google Scholar]
  71. Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA. 71.  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 [Google Scholar]
  72. Kim BH, Kim SY, Nam KH. 72.  2013. Assessing the diverse functions of BAK1 and its homologs in Arabidopsis, beyond BR signaling and PTI responses. Mol. Cells 35:7–16 [Google Scholar]
  73. Korasick DA, McMichael C, Walker KA, Anderson JC, Bednarek SY, Heese A. 73.  2010. Novel functions of stomatal cytokinesis-defective 1 (SCD1) in innate immune responses against bacteria. J. Biol. Chem. 285:23342–50 [Google Scholar]
  74. Kwaaitaal MA, de Vries SC, Russinova E. 74.  2005. Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 226:55–65 [Google Scholar]
  75. Lee AHY, Hurley B, Felsensteiner C, Yea C. 75.  2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLOS Pathog. 9:2e1002523 [Google Scholar]
  76. Lee H, Khatri A, Plotnikov JM, Zhang XC, Sheen J. 76.  2012. Complexity in differential peptide-receptor signaling: response to Segonzac et al. and Mueller et al. commentaries. Plant Cell 24:3177–85 [Google Scholar]
  77. Lee HY, Bowen CH, Popescu GV, Kang HG, Kato N. 77.  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 [Google Scholar]
  78. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ. 78.  2010. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137:467–76 [Google Scholar]
  79. Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M. 79.  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 [Google Scholar]
  80. Li W, Ahn IP, Ning Y, Park CH, Zeng L. 80.  et al. 2012. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol. 159:239–50 [Google Scholar]
  81. Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J. 81.  et al. 2013. Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–87 [Google Scholar]
  82. Liebrand TW, Kombrink A, Zhang Z, Sklenar J, Jones AM. 82.  et al. 2014. Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium. Mol. Plant Pathol. 15:109–17 [Google Scholar]
  83. Liebrand TW, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JH. 83.  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 [Google Scholar]
  84. Liebrand TW, van den Berg GC, Zhang Z, Smit P, Cordewener JH. 84.  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 [Google Scholar]
  85. Lu D, Lin W, Gao X, Wu S, Cheng C. 85.  et al. 2011. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–42 [Google Scholar]
  86. Lu X, Tintor N, Mentzel T, Kombrink E, Boller T. 86.  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 [Google Scholar]
  87. Lu YJ, Schornack S, Spallek T, Geldner N, Chory J. 87.  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 [Google Scholar]
  88. Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C. 88.  et al. 2014. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343:1509–12 [Google Scholar]
  89. Macho AP, Zipfel C. 89.  2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54:263–72 [Google Scholar]
  90. Macnab RM. 90.  2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77–100 [Google Scholar]
  91. Malinovsky FG, Brodersen P, Fiil BK, McKinney LV, Thorgrimsen S. 91.  et al. 2010. Lazarus1, a DUF300 protein, contributes to programmed cell death associated with Arabidopsis acd11 and the hypersensitive response. PLOS ONE 5:e12586 [Google Scholar]
  92. McMichael CM, Reynolds GD, Koch LM, Wang C, Jiang N. 92.  et al. 2013. Mediation of clathrin-dependent trafficking during cytokinesis and cell expansion by Arabidopsis stomatal cytokinesis defective proteins. Plant Cell 25:3910–25 [Google Scholar]
  93. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 93.  2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80 [Google Scholar]
  94. Meyer D, Pajonk S, Micali C, O'Connell R, Schulze-Lefert P. 94.  2009. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. Cell Mol. Biol. 57:986–99 [Google Scholar]
  95. Micali CO, Neumann U, Grunewald D, Panstruga R, O'Connell R. 95.  2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell Microbiol. 13:210–26 [Google Scholar]
  96. Mishina TE, Zeier J. 96.  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 [Google Scholar]
  97. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. 97.  et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:19613–18 [Google Scholar]
  98. Morel JB, Dangl JL. 98.  1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4:671–83 [Google Scholar]
  99. Mukhtar MS, Carvunis A-RR, Dreze M, Epple P, Steinbrenner J. 99.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601 [Google Scholar]
  100. Nekrasov V, Li J, Batoux M, Roux M, Chu ZH. 100.  et al. 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28:3428–38 [Google Scholar]
  101. Nielsen ME, Feechan A, Bohlenius H, Ueda T, Thordal-Christensen H. 101.  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 [Google Scholar]
  102. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY. 102.  2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–23 [Google Scholar]
  103. Nomura K, Mecey C, Lee Y-NN, Imboden LA, Chang JH, He SY. 103.  2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc. Natl. Acad. Sci. USA 108:10774–79 [Google Scholar]
  104. Ntoukakis V, Schwessinger B, Segonzac C, Zipfel C. 104.  2011. Cautionary notes on the use of C-terminal BAK1 fusion proteins for functional studies. Plant Cell 23:3871–78 [Google Scholar]
  105. O'Connell RJ, Panstruga R. 105.  2006. Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171:699–718 [Google Scholar]
  106. Ohno H, Fournier MC, Poy G, Bonifacino JS. 106.  1996. Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J. Biol. Chem. 271:29009–15 [Google Scholar]
  107. Park CJ, Bart R, Chern M, Canlas PE, Bai W, Ronald PC. 107.  2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLOS ONE 5:e9262 [Google Scholar]
  108. Peer WA, Hosein FN, Bandyopadhyay A, Makam SN, Otegui MS. 108.  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 [Google Scholar]
  109. Perez-Gomez J, Moore I. 109.  2007. Plant endocytosis: It is clathrin after all. Curr. Biol. 17:R217–19 [Google Scholar]
  110. Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F. 109a.  et al. 2015. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. In press [Google Scholar]
  111. Richter S, Kientz M, Brumm S, Nielsen ME, Park M. 110.  et al. 2014. Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. Elife 3e02131 [Google Scholar]
  112. Robatzek S, Chinchilla D, Boller T. 111.  2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20:537–42 [Google Scholar]
  113. Romeis T, Ludwig A, Martin R, Jones J. 112.  2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20:5556–67 [Google Scholar]
  114. Ron M, Avni A. 113.  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 [Google Scholar]
  115. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB. 114.  2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–74 [Google Scholar]
  116. Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y. 115.  et al. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–29 [Google Scholar]
  117. Salomon S, Robatzek S. 116.  2006. Induced endocytosis of the receptor kinase FLS2. Plant Signal. Behav. 6:293–95 [Google Scholar]
  118. Scheuring D, Viotti C, Kruger F, Kunzl F, Sturm S. 117.  et al. 2011. Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23:3463–81 [Google Scholar]
  119. Schmidt O, Teis D. 118.  2012. The ESCRT machinery. Curr. Biol. 22:R116–20 [Google Scholar]
  120. Schmidt SM, Kuhn H, Micali C, Liller C, Kwaaitaal M, Panstruga R. 119.  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 [Google Scholar]
  121. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S. 120.  et al. 2010. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285:9444–51 [Google Scholar]
  122. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J. 121.  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 [Google Scholar]
  123. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, Rathjen JP. 122.  2011. Hierarchy and roles of pathogen-associated molecular pattern–induced responses in Nicotiana benthamiana. Plant Physiol. 156:687–99 [Google Scholar]
  124. Serrano M, Robatzek S, Torres M, Kombrink E, Somssich IE. 123.  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 [Google Scholar]
  125. Sharfman M, Bar M, Ehrlich M, Schuster S, Melech-Bonfil S. 124.  et al. 2011. Endosomal signaling of the tomato leucine-rich repeat receptor-like protein LeEix2. Plant J. Cell Mol. Biol. 68:413–23 [Google Scholar]
  126. Sharfman M, Bar M, Schuster S, Leibman M, Avni A. 125.  2014. Sterol-dependent induction of plant defense responses by a microbe-associated molecular pattern from Trichoderma viride. Plant Physiol. 164:819–27 [Google Scholar]
  127. Smith JM, Leslie ME, Robinson SJ, Korasick DA, Zhang T. 126.  et al. 2014. Loss of Arabidopsis thaliana dynamin-related protein 2B reveals separation of innate immune signaling pathways. PLOS Pathog. 10:e1004578 [Google Scholar]
  128. Song WY, Wang GL, Chen LL, Kim HS, Pi LY. 127.  et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–6 [Google Scholar]
  129. Spallek T, Beck M, Ben Khaled S, Salomon S, Bourdais G. 128.  et al. 2013. ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLOS Genet. 9:e1004035 [Google Scholar]
  130. Spallek T, Robatzek S, Gohre V. 129.  2009. How microbes utilize host ubiquitination. Cell. Microbiol. 11:1425–34 [Google Scholar]
  131. Sparkes I, Tolley N, Aller I, Svozil J, Osterrieder A. 130.  et al. 2010. Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 22:1333–43 [Google Scholar]
  132. Speth EB, Imboden L, Hauck P, He SY. 131.  2009. Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol. 149:1824–37 [Google Scholar]
  133. Stegmann M, Anderson RG, Ichimura K, Pecenkova T, Reuter P. 132.  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 [Google Scholar]
  134. Stotz HU, Mitrousia GK, de Wit PJ, Fitt BD. 133.  2014. Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci. 19:491–500 [Google Scholar]
  135. Sun T, Zhang Q, Gao M, Zhang Y. 134.  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 [Google Scholar]
  136. Sun Y, Li L, Macho AP, Han Z, Hu Z. 135.  et al. 2013. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–28 [Google Scholar]
  137. Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J. 136.  2009. Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr. Biol. 19:391–97 [Google Scholar]
  138. Tateda C, Zhang Z, Shrestha J, Jelenska J, Chinchilla D, Greenberg JT. 137.  2014. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26:4171–87 [Google Scholar]
  139. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ. 138.  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 [Google Scholar]
  140. Tilsner J, Amari K, Torrance L. 139.  2011. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39–60 [Google Scholar]
  141. Tintor N, Ross A, Kanehara K, Yamada K, Fan L. 140.  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 [Google Scholar]
  142. Toth R, Gerding-Reimers C, Deeks MJ, Menninger S, Gallegos RM. 141.  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 [Google Scholar]
  143. Trujillo M, Ichimura K, Casais C, Shirasu K. 142.  2008. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18:1396–401 [Google Scholar]
  144. Underwood W, Somerville SC. 143.  2008. Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59:3501–8 [Google Scholar]
  145. Underwood W, Somerville SC. 144.  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 [Google Scholar]
  146. Wang D, Weaver ND, Kesarwani M, Dong X. 145.  2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–40 [Google Scholar]
  147. Wang J, Cai Y, Miao Y, Lam SK, Jiang L. 146.  2009. Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60:3075–83 [Google Scholar]
  148. Weßling R, Epple P, Altmann S, He Y, Yang L. 147.  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 [Google Scholar]
  149. Xin XF, Nomura K, Underwood W, He SY. 148.  2013. Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv. tomato DC3000 infection of Arabidopsis. Mol. Plant-Microbe Interact. 26:861–67 [Google Scholar]
  150. Yun HS, Kwaaitaal M, Kato N, Yi C, Park S. 149.  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 [Google Scholar]
  151. Zeng W, He SY. 150.  2010. A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol. 153:1188–98 [Google Scholar]
  152. Zhang Z, Lenk A, Andersson MX, Gjetting T, Pedersen C. 151.  et al. 2008. A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol. Plant 1:510–27 [Google Scholar]
  153. Zhang Z, Shrestha J, Tateda C, Greenberg JT. 152.  2014. Salicylic acid signaling controls the maturation and localization of the Arabidopsis defense protein ACCELERATED CELL DEATH6. Mol. Plant 7:1365–83 [Google Scholar]
  154. Zhao T, Rui L, Li J, Nishimura M, Vogel J. 153.  et al. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLOS Genet. 11:e1004945 [Google Scholar]
  155. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD. 154.  et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–60 [Google Scholar]
  156. Zipfel C, Robatzek S. 155.  2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi…?. Plant Physiol. 154:551–54 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080614-120347
Loading
/content/journals/10.1146/annurev-phyto-080614-120347
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error