1932

Abstract

At the host–pathogen interface, the protein composition of the plasma membrane (PM) has important implications for how a plant cell perceives and responds to invading microbial pathogens. A plant's ability to modulate its PM composition is critical for regulating the strength, duration, and integration of immune responses. One mechanism by which plant cells reprogram their cell surface is vesicular trafficking, including secretion and endocytosis. These trafficking processes add or remove cargo proteins (such as pattern-recognition receptors, transporters, and other proteins with immune functions) to or from the PM via small, membrane-bound vesicles. Clathrin-coated vesicles (CCVs) that form at the PM and -Golgi network/early endosomes have emerged as the prominent vesicle type in the regulation of plant immune responses. In this review, we discuss the roles of the CCV core, adaptors, and accessory components in plant defense signaling and immunity against various microbial pathogens.

Keyword(s): adaptorCMEdynaminendocytosisFLS2PRR
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080417-045841
2019-08-25
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/phyto/57/1/annurev-phyto-080417-045841.html?itemId=/content/journals/10.1146/annurev-phyto-080417-045841&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adam T, Bouhidel K, Der C, Robert F, Najid A et al. 2012. Constitutive expression of clathrin hub hinders elicitor-induced clathrin-mediated endocytosis and defense gene expression in plant cells. FEBS Lett 586:3293–98
    [Google Scholar]
  2. 2. 
    Adamowski M, Narasimhan M, Kania U, Glanc M, De Jaeger G, Friml J 2018. A functional study of AUXILIN-LIKE1 and 2, two putative clathrin uncoating factors in Arabidopsis. Plant Cell 30:700–16
    [Google Scholar]
  3. 3. 
    Anderson RG, Deb D, Fedkenheuer K, McDowell JM 2015. Recent progress in RXLR effector research. Mol. Plant-Microbe Interact. 28:1063–72
    [Google Scholar]
  4. 4. 
    Antonny B, Burd C, De Camilli P, Chen E, Daumke O et al. 2016. Membrane fission by dynamin: what we know and what we need to know. EMBO J 35:2270–84
    [Google Scholar]
  5. 5. 
    Backues SK, Korasick DA, Heese A, Bednarek SY 2010. The Arabidopsis dynamin-related protein2 family is essential for gametophyte development. Plant Cell 22:3218–31
    [Google Scholar]
  6. 6. 
    Baisa GA, Mayers JR, Bednarek SY 2013. Budding and braking news about clathrin-mediated endocytosis. Curr. Opin. Plant Biol. 16:718–25
    [Google Scholar]
  7. 7. 
    Banbury DN, Oakley JD, Sessions RB, Banting G 2003. Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. J. Biol. Chem. 278:12022–28
    [Google Scholar]
  8. 8. 
    Bar M, Avni A. 2009. EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J 59:600–11
    [Google Scholar]
  9. 9. 
    Bar M, Schuster S, Leibman M, Ezer R, Avni A 2014. The function of EHD2 in endocytosis and defense signaling is affected by SUMO. Plant Mol. Biol. 84:509–18
    [Google Scholar]
  10. 10. 
    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
    [Google Scholar]
  11. 11. 
    Bashline L, Li S, Zhu X, Gu Y 2015. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. PNAS 112:12870–75
    [Google Scholar]
  12. 12. 
    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
    [Google Scholar]
  13. 13. 
    Bednarek SY, Backues SK. 2010. Plant dynamin-related protein families DRP1 and DRP2 in plant development. Biochem. Soc. Trans. 38:797–806
    [Google Scholar]
  14. 14. 
    Ben Khaled S, Postma J, Robatzek S 2015. A moving view: subcellular trafficking processes in pattern recognition receptor–triggered plant immunity. Annu. Rev. Phytopathol. 53:379–402
    [Google Scholar]
  15. 15. 
    Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR et al. 2010. Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. PNAS 107:14502–7
    [Google Scholar]
  16. 16. 
    Brandizzi F, Barlowe C. 2013. Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14:382–92
    [Google Scholar]
  17. 17. 
    Büttner D. 2016. Behind the lines-actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40:894–937
    [Google Scholar]
  18. 18. 
    Chaparro-Garcia A, Schwizer S, Sklenar J, Yoshida K, Petre B et al. 2015. Phytophthora infestans RXLR-WY effector AVR3a associates with Dynamin-Related Protein 2 required for endocytosis of the plant pattern recognition receptor FLS2. PLOS ONE 10:e0137071
    [Google Scholar]
  19. 19. 
    Chen X, Irani NG, Friml J 2011. Clathrin-mediated endocytosis: the gateway into plant cells. Curr. Opin. Plant Biol. 14:674–82
    [Google Scholar]
  20. 20. 
    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
    [Google Scholar]
  21. 21. 
    Chisholm ST, Coaker G, Day B, Staskawicz BJ 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–14
    [Google Scholar]
  22. 22. 
    Choi S-W, 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
    [Google Scholar]
  23. 23. 
    Claus LAN, Savatin DV, Russinova E 2018. The crossroads of receptor-mediated signaling and endocytosis in plants. J. Integr. Plant Biol. 60:827–40
    [Google Scholar]
  24. 24. 
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52
    [Google Scholar]
  25. 25. 
    Cui H, Tsuda K, Parker JE 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
    [Google Scholar]
  26. 26. 
    Cui Y, Li X, Yu M, Li R, Fan L et al. 2018. Sterols regulate endocytic pathways during flg22-induced defense responses in Arabidopsis. Development 145:dev165688
    [Google Scholar]
  27. 27. 
    De Craene J-O, Ripp R, Lecompte O, Thompson JD, Poch O, Friant S 2012. Evolutionary analysis of the ENTH/ANTH/VHS protein superfamily reveals a coevolution between membrane trafficking and metabolism. BMC Genom 13:297
    [Google Scholar]
  28. 28. 
    Dejonghe W, Kuenen S, Mylle E, Vasileva M, Keech O et al. 2016. Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification. Nat. Commun. 7:11710
    [Google Scholar]
  29. 29. 
    Di Rubbo S, Irani NG, Kim SY, Xu Z-Y, Gadeyne A et al. 2013. The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis. Plant Cell 25:2986–97
    [Google Scholar]
  30. 30. 
    Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11:539–48
    [Google Scholar]
  31. 31. 
    Doehlemann G, Hemetsberger C. 2013. Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol 198:1001–16
    [Google Scholar]
  32. 32. 
    Du Y, Tejos R, Beck M, Himschoot E, Li H et al. 2013. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. PNAS 110:7946–51
    [Google Scholar]
  33. 33. 
    Dubeaux G, Vert G. 2017. Zooming into plant ubiquitin-mediated endocytosis. Curr. Opin. Plant Biol. 40:56–62
    [Google Scholar]
  34. 34. 
    Falbel TG, Koch LM, Nadeau J, Segui-Simarro JM, Sack FD, Bednarek SY 2003. SCD1 is required for cell cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development 130:4495
    [Google Scholar]
  35. 35. 
    Fan L, Hao H, Xue Y, Zhang L, Song K et al. 2013. Dynamic analysis of Arabidopsis AP2 σ subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140:3826–37
    [Google Scholar]
  36. 36. 
    Fang C, Gao M-J, Miao Y-S, Yuan Y-X, Wang M-Y et al. 2010. Plasma membrane localization and potential endocytosis of constitutively expressed XA21 proteins in transgenic rice. Mol. Plant 3:917–26
    [Google Scholar]
  37. 37. 
    Faulkner C. 2015. A cellular backline: specialization of host membranes for defence. J. Exp. Bot. 66:1565–71
    [Google Scholar]
  38. 38. 
    Gadeyne A, Sánchez-Rodríguez C, Vanneste S, Di Rubbo S, Zauber H et al. 2014. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 156:691–704
    [Google Scholar]
  39. 39. 
    Gendre D, Jonsson K, Boutté Y, Bhalerao RP 2015. Journey to the cell surface—the central role of the trans-Golgi network in plants. Protoplasma 252:385–98
    [Google Scholar]
  40. 40. 
    Geng X, Jin L, Shimada M, Kim MG, Mackey D 2014. The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta 240:1149–65
    [Google Scholar]
  41. 41. 
    Gu Y, Zavaliev R, Dong X 2017. Membrane trafficking in plant immunity. Mol. Plant 10:1026–34
    [Google Scholar]
  42. 42. 
    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
    [Google Scholar]
  43. 43. 
    Hatsugai N, Hillmer R, Yamaoka S, Hara-Nishimura I, Katagiri F 2016. The μ subunit of Arabidopsis adaptor protein-2 is involved in effector-triggered immunity mediated by membrane-localized resistance proteins. Mol. Plant-Microbe Interact. 29:345–51
    [Google Scholar]
  44. 44. 
    He Y, Zhou J, Shan L, Meng X 2018. Plant cell surface receptor-mediated signaling—a common theme amid diversity. J. Cell Sci. 131:jcs209353
    [Google Scholar]
  45. 45. 
    Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22
    [Google Scholar]
  46. 46. 
    Hirst J, Schlacht A, Norcott JP, Traynor D, Bloomfield G et al. 2014. Characterization of TSET, an ancient and widespread membrane trafficking complex. eLife 3:e02866
    [Google Scholar]
  47. 47. 
    Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G et al. 2003. A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol. Biol. 53:261–65
    [Google Scholar]
  48. 48. 
    Houston K, Tucker MR, Chowdhury J, Shirley N, Little A 2016. The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front. Plant Sci. 7:984
    [Google Scholar]
  49. 49. 
    Irani NG, Di Rubbo S, Mylle E, Van den Begin J, Schneider-Pizoń J et al. 2012. Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat. Chem. Biol. 8:583–89
    [Google Scholar]
  50. 50. 
    Johnson A, Vert G. 2017. Single event resolution of plant plasma membrane protein endocytosis by TIRF microscopy. Front. Plant Sci. 8:612
    [Google Scholar]
  51. 51. 
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  52. 52. 
    Jones JDG, Vance RE, Dangl JL 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395
    [Google Scholar]
  53. 53. 
    Kadota Y, Liebrand TWH, Goto Y, Sklenar J, Derbyshire P et al. 2018. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol 9:2160–75
    [Google Scholar]
  54. 54. 
    Kadota Y, Shirasu K, Zipfel C 2015. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56:1472–80
    [Google Scholar]
  55. 55. 
    Kirchhausen T, Owen D, Harrison SC 2014. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6:a016725
    [Google Scholar]
  56. 56. 
    Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T et al. 2011. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–31
    [Google Scholar]
  57. 57. 
    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
    [Google Scholar]
  58. 58. 
    Lam BC, Sage TL, Bianchi F, Blumwald E 2001. Role of SH3 domain-containing proteins in clathrin-mediated vesicle trafficking in Arabidopsis. Plant Cell 13:2499–512
    [Google Scholar]
  59. 59. 
    LaMontagne ED, Heese A. 2017. Trans-Golgi network/early endosome: a central sorting station for cargo proteins in plant immunity. Curr. Opin. Plant Biol. 40:114–21
    [Google Scholar]
  60. 60. 
    Larson ER, Van Zelm E, Roux C, Marion-Poll A, Blatt MR 2017. Clathrin heavy chain subunits coordinate endo- and exocytic traffic and affect stomatal movement. Plant Physiol 175:708–20
    [Google Scholar]
  61. 61. 
    Lee HY, Bowen CH, Popescu GV, Kang H-G, 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
    [Google Scholar]
  62. 62. 
    Leslie ME, Heese A. 2017. Quantitative analysis of ligand-induced endocytosis of FLAGELLIN-SENSING 2 using automated image segmentation. Plant Pattern Recognition Receptors: Methods and Protocols L Shan, P He 39–54 New York: Springer
    [Google Scholar]
  63. 63. 
    Leslie ME, Rogers SW, Heese A 2016. Increased callose deposition in plants lacking DYNAMIN-RELATED PROTEIN 2B is dependent upon POWDERY MILDEWRESISTANT 4. Plant Signal. Behav 11:e1244594
    [Google Scholar]
  64. 64. 
    Li B, Lu D, Shan L 2014. Ubiquitination of pattern recognition receptors in plant innate immunity. Mol. Plant Pathol. 15:737–46
    [Google Scholar]
  65. 65. 
    Li X, Pan SQ. 2017. Agrobacterium delivers VirE2 protein into host cells via clathrin-mediated endocytosis. Sci. Adv. 3:e1601528
    [Google Scholar]
  66. 66. 
    Liu S-H, Wong ML, Craik CS, Brodsky FM 1995. Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell 83:257–67
    [Google Scholar]
  67. 67. 
    Lo Presti L, Kahmann R 2017. How filamentous plant pathogen effectors are translocated to host cells. Curr. Opin. Plant Biol. 38:19–24
    [Google Scholar]
  68. 68. 
    Lu D, Lin W, Gao X, Wu S, Cheng C et al. 2011. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–42
    [Google Scholar]
  69. 69. 
    Mayers JR, Hu T, Wang C, Cárdenas JJ, Tan Y et al. 2017. SCD1 and SCD2 form a complex that functions with the exocyst and RabE1 in exocytosis and cytokinesis. Plant Cell 29:2610–25
    [Google Scholar]
  70. 70. 
    Mbengue M, Bourdais G, Gervasi F, Beck M, Zhou J et al. 2016. Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases. PNAS 113:11034–39
    [Google Scholar]
  71. 71. 
    McGettrick AF, O'Neill LAJ. 2010. Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr. Opin. Immunol. 22:20–27
    [Google Scholar]
  72. 72. 
    McMichael CM, Bednarek SY. 2013. Cytoskeletal and membrane dynamics during higher plant cytokinesis. New Phytol 197:1039–57
    [Google Scholar]
  73. 73. 
    McMichael CM, Reynolds GD, Koch LM, Wang C, Jiang N 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]
  74. 74. 
    Melotto M, Zhang L, Oblessuc PR, He SY 2017. Stomatal defense a decade later. Plant Physiol 174:561–71
    [Google Scholar]
  75. 75. 
    Merrifield CJ, Kaksonen M. 2014. Endocytic accessory factors and regulation of clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 6:a016733
    [Google Scholar]
  76. 76. 
    Moreno AA, Mukhtar MS, Blanco F, Boatwright JL, Moreno I et al. 2012. IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLOS ONE 7:e31944
    [Google Scholar]
  77. 77. 
    Mukhtar MS, Carvunis A-R, 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
    [Google Scholar]
  78. 78. 
    Myers MD, Payne GS 2013. Clathrin, adaptors and disease: insights from the yeast Saccharomyces cerevisiae. Front. Biosci 18:862–91
    [Google Scholar]
  79. 79. 
    Nagel M-K, Kalinowska K, Vogel K, Reynolds GD, Wu Z et al. 2017. Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3. PNAS 114:E7197–204
    [Google Scholar]
  80. 80. 
    Ortiz-Morea FA, Savatin DV, Dejonghe W, Kumar R, Luo Y et al. 2016. Danger-associated peptide signaling in Arabidopsis requires clathrin. PNAS 113:11028–33
    [Google Scholar]
  81. 81. 
    Paez Valencia J, Goodman K, Otegui MS 2016. Endocytosis and endosomal trafficking in plants. Annu. Rev. Plant Biol. 67:309–35
    [Google Scholar]
  82. 82. 
    Park C-J, Wei T, Sharma R, Ronald PC 2017. Overexpression of rice auxilin-like protein, XB21, induces necrotic lesions, up-regulates endocytosis-related genes, and confers enhanced resistance to Xanthomonas oryzae pv. oryzae. Rice 10:27
    [Google Scholar]
  83. 83. 
    Park M, Song K, Reichardt I, Kim H, Mayer U et al. 2013. Arabidopsis μ-adaptin subunit AP1M of adaptor protein complex 1 mediates late secretory and vacuolar traffic and is required for growth. PNAS 110:10318–23
    [Google Scholar]
  84. 84. 
    Peng Y, van Wersch R, Zhang Y 2017. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant-Microbe Interact. 31:403–9
    [Google Scholar]
  85. 85. 
    Preta G, Cronin JG, Sheldon IM 2015. Dynasore—not just a dynamin inhibitor. Cell Commun. Signal. 13:24
    [Google Scholar]
  86. 86. 
    Qi J, Wang J, Gong Z, Zhou J-M 2017. Apoplastic ROS signaling in plant immunity. Curr. Opin. Plant Biol. 38:92–100
    [Google Scholar]
  87. 87. 
    Qiao Y, Jiang W, Lee J, Park B, Choi M-S et al. 2010. SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit μ1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol 185:258–74
    [Google Scholar]
  88. 88. 
    Reynolds GD, August B, Bednarek SY 2014. Preparation of enriched plant clathrin-coated vesicles by differential and density gradient centrifugation. Plant Endosomes: Methods and Protocols MS Otegui 163–77 New York: Springer
    [Google Scholar]
  89. 89. 
    Reynolds GD, Wang C, Pan J, Bednarek SY 2018. Inroads into internalization: five years of endocytic exploration. Plant Physiol 176:208–18
    [Google Scholar]
  90. 90. 
    Robinson DG, Neuhaus J-M. 2016. Receptor-mediated sorting of soluble vacuolar proteins: myths, facts, and a new model. J. Exp. Bot. 67:4435–49
    [Google Scholar]
  91. 91. 
    Robinson DG, Pimpl P. 2014. Clathrin and post-Golgi trafficking: a very complicated issue. Trends Plant Sci 19:134–39
    [Google Scholar]
  92. 92. 
    Robinson MS. 2015. Forty years of clathrin-coated vesicles. Traffic 16:1210–38
    [Google Scholar]
  93. 93. 
    Ron M, 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
    [Google Scholar]
  94. 94. 
    Rosquete MR, Drakakaki G. 2018. Plant TGN in the stress response: a compartmentalized overview. Curr. Opin. Plant Biol. 46:122–29
    [Google Scholar]
  95. 95. 
    Sánchez-Rodríguez C, Shi Y, Kesten C, Zhang D, Sancho-Andrés G et al. 2018. The cellulose synthases are cargo of the TPLATE adaptor complex. Mol. Plant 11:346–49
    [Google Scholar]
  96. 96. 
    Sánchez-Vallet A, Fouché S, Fudal I, Hartmann FE, Soyer JL et al. 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annu. Rev. Phytopathol. 56:21–40
    [Google Scholar]
  97. 97. 
    Sauer M, Delgadillo MO, Zouhar J, Reynolds GD, Pennington JG et al. 2013. MTV1 and MTV4 encode plant-specific ENTH and ARF GAP proteins that mediate clathrin-dependent trafficking of vacuolar cargo from the trans-Golgi network. Plant Cell 25:2217–35
    [Google Scholar]
  98. 98. 
    Scheele U, Holstein SEH. 2002. Functional evidence for the identification of an Arabidopsis clathrin light chain polypeptide. FEBS Lett 514:355–60
    [Google Scholar]
  99. 99. 
    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
    [Google Scholar]
  100. 100. 
    Schneider R, Hanak T, Persson S, Voigt CA 2016. Cellulose and callose synthesis and organization in focus, what's new?. Curr. Opin. Plant Biol. 34:9–16
    [Google Scholar]
  101. 101. 
    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 68:413–23
    [Google Scholar]
  102. 102. 
    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 Pathogens 10:e1004578
    [Google Scholar]
  103. 103. 
    Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A 2014. Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol 164:440–54
    [Google Scholar]
  104. 104. 
    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
    [Google Scholar]
  105. 105. 
    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
    [Google Scholar]
  106. 106. 
    Tang D, Ade J, Frye CA, Innes RW 2006. A mutation in the GTP hydrolysis site of Arabidopsis dynamin-related protein 1E confers enhanced cell death in response to powdery mildew infection. Plant J 47:75–84
    [Google Scholar]
  107. 107. 
    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
    [Google Scholar]
  108. 108. 
    Taylor NG. 2011. A role for Arabidopsis dynamin related proteins DRP2A/B in endocytosis; DRP2 function is essential for plant growth. Plant Mol. Biol. 76:117–29
    [Google Scholar]
  109. 109. 
    Tinevez J-Y, Perry N, Schindelin J, Hoopes GM, Reynolds GD et al. 2017. TrackMate: an open and extensible platform for single-particle tracking. Methods 115:80–90
    [Google Scholar]
  110. 110. 
    Tsuda K, Katagiri F. 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13:459–65
    [Google Scholar]
  111. 111. 
    Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F 2009. Network properties of robust immunity in plants. PLOS Genet 5:e1000772
    [Google Scholar]
  112. 112. 
    Uemura T. 2016. Physiological roles of plant post-Golgi transport pathways in membrane trafficking. Plant Cell Physiol 57:2013–19
    [Google Scholar]
  113. 113. 
    Underwood W. 2016. Contributions of host cellular trafficking and organization to the outcomes of plant-pathogen interactions. Semin. Cell Dev. Biol. 56:163–73
    [Google Scholar]
  114. 114. 
    Viotti C, Bubeck J, Stierhof Y-D, Krebs M, Langhans M et al. 2010. Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–57
    [Google Scholar]
  115. 115. 
    Wang C, Hu T, Yan X, Meng T, Wang Y et al. 2016. Differential regulation of clathrin and its adaptor proteins during membrane recruitment for endocytosis. Plant Physiol 171:215–29
    [Google Scholar]
  116. 116. 
    Wang C, Yan X, Chen Q, Jiang N, Fu W et al. 2013. Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. Plant Cell 25:499–516
    [Google Scholar]
  117. 117. 
    Wang C, Zhu M, Duan L, Yu H, Chang X et al. 2015. Lotus japonicus clathrin heavy chain1 is associated with Rho-Like GTPase ROP6 and involved in nodule formation. Plant Physiol 167:1497–510
    [Google Scholar]
  118. 118. 
    Wang D, Dong X. 2011. A highway for war and peace: the secretory pathway in plant-microbe interactions. Mol. Plant 4:581–87
    [Google Scholar]
  119. 119. 
    Wang D, Weaver ND, Kesarwani M, Dong X 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–40
    [Google Scholar]
  120. 120. 
    Wang L, Li H, Lv X, Chen T, Li R et al. 2015. Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol. Plant 8:1334–49
    [Google Scholar]
  121. 121. 
    Wang W-M, Liu P-Q, Xu Y-J, Xiao S 2016. Protein trafficking during plant innate immunity. J. Integr. Plant Biol. 58:284–98
    [Google Scholar]
  122. 122. 
    Wang X, Cai Y, Wang H, Zeng Y, Zhuang X et al. 2014. Trans-Golgi network-located AP1 gamma adaptins mediate dileucine motif-directed vacuolar targeting in Arabidopsis. Plant Cell 26:4102–18
    [Google Scholar]
  123. 123. 
    Wang Y, Wang Y. 2017. Trick or treat: microbial pathogens evolved apoplastic effectors modulating plant susceptibility to infection. Mol. Plant-Microbe Interact. 31:6–12
    [Google Scholar]
  124. 124. 
    Webling 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
    [Google Scholar]
  125. 125. 
    Wu G, Cui X, Chen H, Renaud JB, Yu K et al. 2018. Dynamin-like proteins of endocytosis in plants are coopted by potyviruses to enhance virus infection. J. Virol. 92:e01320–18
    [Google Scholar]
  126. 126. 
    Wu G, Liu S, Zhao Y, Wang W, Kong Z, Tang D 2015. ENHANCED DISEASE RESISTANCE4 associates with CLATHRIN HEAVY CHAIN2 and modulates plant immunity by regulating relocation of EDR1 in Arabidopsis. Plant Cell 27:857–73
    [Google Scholar]
  127. 127. 
    Xie M, Zhang J, Tschaplinski TJ, Tuskan GA, Chen J-G, Muchero W 2018. Regulation of lignin biosynthesis and its role in growth-defense tradeoffs. Front. Plant Sci. 9:1427
    [Google Scholar]
  128. 128. 
    Xin X-F, Kvitko B, He SY 2018. Pseudomonas syringae: what it takes to be a pathogen. Nat. Rev. Microbiol. 16:316–28
    [Google Scholar]
  129. 129. 
    Yu Q, Zhang Y, Wang J, Yan X, Wang C et al. 2016. Clathrin-mediated auxin efflux and maxima regulate hypocotyl hook formation and light-stimulated hook opening in Arabidopsis. Mol. Plant 9:101–12
    [Google Scholar]
  130. 130. 
    Yu X, Feng B, He P, Shan L 2017. From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 55:109–37
    [Google Scholar]
  131. 131. 
    Yun HS, Kwon C. 2017. Vesicle trafficking in plant immunity. Curr. Opin. Plant Biol. 40:34–42
    [Google Scholar]
  132. 132. 
    Zeng M-H, Liu S-H, Yang M-X, Zhang Y-J, Liang J-Y et al. 2013. Characterization of a gene encoding clathrin heavy chain in maize up-regulated by salicylic acid, abscisic acid and high boron supply. Int. J. Mol. Sci. 14:15179–98
    [Google Scholar]
  133. 133. 
    Zhang Y, Persson S, Hirst J, Robinson MS, van Damme D, Sánchez-Rodríguez C 2015. Change your Tplate, change your fate: plant CME and beyond. Trends Plant Sci 20:41–48
    [Google Scholar]
  134. 134. 
    Zhang Z, Lenk A, Andersson MX, 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
    [Google Scholar]
  135. 135. 
    Zhang Z, Song Y, Liu C-M, Thomma BPHJ 2014. Mutational analysis of the Ve1 immune receptor that mediates Verticillium resistance in tomato. PLOS ONE 9:e99511
    [Google Scholar]
  136. 136. 
    Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG et al. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–77
    [Google Scholar]
  137. 137. 
    Zouhar J, Sauer M. 2014. Helping hands for budding prospects: ENTH/ANTH/VHS accessory proteins in endocytosis, vacuolar transport, and secretion. Plant Cell 26:4232–44
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-080417-045841
Loading
/content/journals/10.1146/annurev-phyto-080417-045841
Loading

Data & Media loading...

  • 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