1932

Abstract

Membrane trafficking pathways play a prominent role in plant immunity. The endomembrane transport system coordinates membrane-bound cellular organelles to ensure that immunological components are utilized effectively during pathogen resistance. Adapted pathogens and pests have evolved to interfere with aspects of membrane transport systems to subvert plant immunity. To do this, they secrete virulence factors known as effectors, many of which converge on host membrane trafficking routes. The emerging paradigm is that effectors redundantly target every step of membrane trafficking from vesicle budding to trafficking and membrane fusion. In this review, we focus on the mechanisms adopted by plant pathogens to reprogram host plant vesicle trafficking, providing examples of effector-targeted transport pathways and highlighting key questions for the field to answer moving forward.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021622-123232
2023-09-05
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/phyto/61/1/annurev-phyto-021622-123232.html?itemId=/content/journals/10.1146/annurev-phyto-021622-123232&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abdul Malik NA, Kumar IS, Nadarajah K 2020. Elicitor and receptor molecules: orchestrators of plant defense and immunity. Int. J. Mol. Sci. 21:3963
    [Google Scholar]
  2. 2.
    Adachi H, Contreras MP, Harant A, Wu CH, Derevnina L et al. 2019. An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8:e49956
    [Google Scholar]
  3. 3.
    Afzal AJ, da Cunha L, Mackey D. 2011. Separable fragments and membrane tethering of Arabidopsis RIN4 regulate its suppression of PAMP-triggered immunity. Plant Cell 23:3798–811
    [Google Scholar]
  4. 4.
    Asaoka R, Uemura T, Ito J, Fujimoto M, Ito E et al. 2013. Arabidopsis RABA1 GTPases are involved in transport between the trans-Golgi network and the plasma membrane, and are required for salinity stress tolerance. Plant J. 73:240–49
    [Google Scholar]
  5. 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
    [Google Scholar]
  6. 6.
    Baena G, Xia L, Waghmare S, Karnik R. 2022. SNARE SYP132 mediates divergent traffic of plasma membrane H+-ATPase AHA1 and antimicrobial PR1 during bacterial pathogenesis. Plant Physiol. 189:1639–61
    [Google Scholar]
  7. 7.
    Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R et al. 2009. The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall–associated defense responses. Mol. Plant-Microbe Interact. 22:655–64
    [Google Scholar]
  8. 8.
    Bayless AM, Smith JM, Song J, McMinn PH, Teillet A et al. 2016. Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1. PNAS 113:E7375–82
    [Google Scholar]
  9. 9.
    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]
  10. 10.
    Bi G, Su M, Li N, Liang Y, Dang S et al. 2021. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184:3528–41.e12
    [Google Scholar]
  11. 11.
    Boyes DC, Nam J, Dangl JL. 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. PNAS 95:15849–54
    [Google Scholar]
  12. 12.
    Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH et al. 2015. Rerouting of plant late endocytic trafficking toward a pathogen interface. Traffic 16:204–26
    [Google Scholar]
  13. 13.
    Bozkurt TO, Kamoun S. 2020. The plant–pathogen haustorial interface at a glance. J. Cell Sci. 133:jcs237958
    [Google Scholar]
  14. 14.
    Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M et al. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. PNAS 108:20832–37
    [Google Scholar]
  15. 15.
    Caillaud MC, Wirthmueller L, Sklenar J, Findlay K, Piquerez SJ et al. 2014. The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLOS Pathog. 10:e1004496
    [Google Scholar]
  16. 16.
    Cao W-L, Yu Y, Li M-Y, Luo J, Wang R-S et al. 2019. OsSYP121 accumulates at fungal penetration sites and mediates host resistance to rice blast. Plant Physiol. 179:1330–42
    [Google Scholar]
  17. 17.
    Chang JH, Desveaux D, Creason AL. 2014. The ABCs and 123s of bacterial secretion systems in plant pathogenesis. Annu. Rev. Phytopathol. 52:317–45
    [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 J, Chen S, Xu C, Yang H, Achom M, Wang X. 2022. A key virulence effector from cyst nematodes targets host autophagy to promote nematode parasitism. New Phytol. 237:41374–90
    [Google Scholar]
  20. 20.
    Cheng F-Y, Zamski E, Guo W-W, Pharr DM, Williamson JD. 2009. Salicylic acid stimulates secretion of the normally symplastic enzyme mannitol dehydrogenase: a possible defense against mannitol-secreting fungal pathogens. Planta 230:1093–103
    [Google Scholar]
  21. 21.
    Cheng X, Wang A. 2017. The potyvirus silencing suppressor protein VPg mediates degradation of SGS3 via ubiquitination and autophagy pathways. J. Virol. 91:e01478–16
    [Google Scholar]
  22. 22.
    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
    [Google Scholar]
  23. 23.
    Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E et al. 2003. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–77
    [Google Scholar]
  24. 24.
    Collins RN. 2003. Rab and ARF GTPase regulation of exocytosis. Mol. Membr. Biol. 20:105–15
    [Google Scholar]
  25. 25.
    Contreras MP, Pai H, Tumtas Y, Duggan C, Yuen ELH et al. 2022. Sensor NLR immune proteins activate oligomerization of their NRC helper. bioRxiv 489342 . https://doi.org/10.1101/2022.04.25.489342
    [Crossref]
  26. 26.
    Csorba T, Lozsa R, Hutvagner G, Burgyan J. 2010. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J. 62:463–72
    [Google Scholar]
  27. 27.
    Cunnac S, Lindeberg M, Collmer A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12:53–60
    [Google Scholar]
  28. 28.
    Dagdas YF, Belhaj K, Maqbool A, Chaparro-Garcia A, Pandey P et al. 2016. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. eLife 5:e10856
    [Google Scholar]
  29. 29.
    Dagdas YF, Pandey P, Tumtas Y, Sanguankiattichai N, Belhaj K et al. 2018. Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen. eLife 7:e37476
    [Google Scholar]
  30. 30.
    Day B, Henty JL, Porter KJ, Staiger CJ. 2011. The pathogen-actin connection: a platform for defense signaling in plants. Annu. Rev. Phytopathol. 49:483–506
    [Google Scholar]
  31. 31.
    DeFalco TA, Zipfel C. 2021. Molecular mechanisms of early plant pattern-triggered immune signaling. Mol. Cell 81:4346
    [Google Scholar]
  32. 32.
    Derevnina L, Contreras MP, Adachi H, Upson J, Vergara Cruces A et al. 2021. Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. PLOS Biol. 19:e3001136
    [Google Scholar]
  33. 33.
    Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K. 2006. Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–30
    [Google Scholar]
  34. 34.
    Du Y, Mpina MH, Birch PR, Bouwmeester K, Govers F. 2015. Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiol. 169:1975–90
    [Google Scholar]
  35. 35.
    Du Y, Overdijk EJR, Berg JA, Govers F, Bouwmeester K. 2018. Solanaceous exocyst subunits are involved in immunity to diverse plant pathogens. J. Exp. Bot. 69:655–66
    [Google Scholar]
  36. 36.
    Duggan C, Moratto E, Savage Z, Hamilton E, Adachi H et al. 2021. Dynamic localization of a helper NLR at the plant-pathogen interface underpins pathogen recognition. PNAS 118:e2104997118
    [Google Scholar]
  37. 37.
    El Kasmi F, Chung EH, Anderson RG, Li J, Wan L et al. 2017. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. PNAS 114:E7385–94
    [Google Scholar]
  38. 38.
    Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PR. 2012. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24:5142–58
    [Google Scholar]
  39. 39.
    Fakhree MAA, Blum C, Claessens M. 2019. Shaping membranes with disordered proteins. Arch. Biochem. Biophys. 677:108163
    [Google Scholar]
  40. 40.
    Fan L, Li R, Pan J, Ding Z, Lin J. 2015. Endocytosis and its regulation in plants. Trends Plant Sci. 20:388–97
    [Google Scholar]
  41. 41.
    Fu S, Xu Y, Li C, Li Y, Wu J, Zhou X. 2018. Rice stripe virus interferes with S-acylation of remorin and induces its autophagic degradation to facilitate virus infection. Mol. Plant 11:269–87
    [Google Scholar]
  42. 42.
    Fuchs R, Kopischke M, Klapprodt C, Hause G, Meyer AJ et al. 2016. Immobilized subpopulations of leaf epidermal mitochondria mediate PENETRATION2-dependent pathogen entry control in Arabidopsis. Plant Cell 28:130–45
    [Google Scholar]
  43. 43.
    Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K et al. 2015. Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J. 83:875–87
    [Google Scholar]
  44. 44.
    Fujiwara M, Uemura T, Ebine K, Nishimori Y, Ueda T et al. 2014. Interactomics of Qa-SNARE in Arabidopsis thaliana. Plant Cell Physiol. 55:781–89
    [Google Scholar]
  45. 45.
    Ge S, Zhang RX, Wang YF, Sun P, Chu J et al. 2022. The Arabidopsis Rab protein RABC1 affects stomatal development by regulating lipid droplet dynamics. Plant Cell 34:114274–92
    [Google Scholar]
  46. 46.
    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
    [Google Scholar]
  47. 47.
    Guo M, Kim P, Li G, Elowsky CG, Alfano JR. 2016. A bacterial effector co-opts calmodulin to target the plant microtubule network. Cell Host Microbe 19:67–78
    [Google Scholar]
  48. 48.
    Hadlington JL, Denecke J. 2000. Sorting of soluble proteins in the secretory pathway of plants. Curr. Opin. Plant Biol. 3:461–68
    [Google Scholar]
  49. 49.
    Hafrén A, Macia J-L, Love AJ, Milner JJ, Drucker M, Hofius D. 2017. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. PNAS 114:E2026–35
    [Google Scholar]
  50. 50.
    Hafrén A, Üstün S, Hochmuth A, Svenning S, Johansen T, Hofius D. 2018. Turnip mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiol. 176:649–62
    [Google Scholar]
  51. 51.
    Holden S, Bergum M, Green P, Bettgenhaeuser J, Hernández-Pinzón I et al. 2022. A lineage-specific Exo70 is required for receptor kinase–mediated immunity in barley. Sci. Adv. 8:eabn7258
    [Google Scholar]
  52. 52.
    Hu M, Qi J, Bi G, Zhou JM. 2020. Bacterial effectors induce oligomerization of immune receptor ZAR1 in vivo. Mol. Plant 13:793–801
    [Google Scholar]
  53. 53.
    Hyodo K, Kaido M, Okuno T. 2014. Traffic jam on the cellular secretory pathway generated by a replication protein from a plant RNA virus. Plant Signal. Behav. 9:e28644
    [Google Scholar]
  54. 54.
    Hyodo K, Mine A, Taniguchi T, Kaido M, Mise K et al. 2013. ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus. J. Virol. 87:163–76
    [Google Scholar]
  55. 55.
    Ibrahim T, Khandare V, Mirkin FG, Tumtas Y, Bubeck D, Bozkurt TO. 2022. AF2-multimer guided high accuracy prediction of typical and atypical ATG8 binding motifs. bioRxiv 509395 . https://doi.org/10.1101/2022.09.25.509395
    [Crossref]
  56. 56.
    Ivanov R, Vert G. 2021. Endocytosis in plants: peculiarities and roles in the regulated trafficking of plant metal transporters. Biol. Cell 113:1–13
    [Google Scholar]
  57. 57.
    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:e1004232
    [Google Scholar]
  58. 58.
    Kim H, O'Connell R, Maekawa-Yoshikawa M, Uemura T, Neumann U, Schulze-Lefert P. 2014. The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes. Plant J. 79:835–47
    [Google Scholar]
  59. 59.
    Kwon C, Neu C, Pajonk S, Yun HS, Lipka U et al. 2008. Co-option of a default secretory pathway for plant immune responses. Nature 451:835–40
    [Google Scholar]
  60. 60.
    Lal NK, Thanasuwat B, Huang P-J, Cavanaugh KA, Carter A et al. 2020. Phytopathogen effectors use multiple mechanisms to manipulate plant autophagy. Cell Host Microbe 28:558–71.e6
    [Google Scholar]
  61. 61.
    Lam SK, Siu CL, Hillmer S, Jang S, An G et al. 2007. Rice SCAMP1 defines clathrin-coated, trans-Golgi–located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319
    [Google Scholar]
  62. 62.
    Lamason RL, Welch MD. 2017. Actin-based motility and cell-to-cell spread of bacterial pathogens. Curr. Opin. Microbiol. 35:48–57
    [Google Scholar]
  63. 63.
    Langin G, Gouguet P, Üstün S. 2020. Microbial effector proteins—a journey through the proteolytic landscape. Trends Microbiol. 28:523–35
    [Google Scholar]
  64. 64.
    Leary AY, Savage Z, Tumtas Y, Bozkurt TO. 2019. Contrasting and emerging roles of autophagy in plant immunity. Curr. Opin. Plant Biol. 52:46–53
    [Google Scholar]
  65. 65.
    Lee AH-Y, Hurley B, Felsensteiner C, Yea C, Ckurshumova W et al. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLOS Pathog. 8:e1002523
    [Google Scholar]
  66. 66.
    Leong JX, Langin G, Ustun S. 2022. Selective autophagy: adding precision in plant immunity. Essays Biochem. 66:189–206
    [Google Scholar]
  67. 67.
    Leong JX, Raffeiner M, Spinti D, Langin G, Franz-Wachtel M et al. 2022. A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component. EMBO J. 41:e110352
    [Google Scholar]
  68. 68.
    Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469:323–35
    [Google Scholar]
  69. 69.
    Li P, Day B. 2019. Battlefield cytoskeleton: turning the tide on plant immunity. Mol. Plant-Microbe Interact. 32:25–34
    [Google Scholar]
  70. 70.
    Li T, Ai G, Fu X, Liu J, Zhu H et al. 2022. A Phytophthora capsici RXLR effector manipulates plant immunity by targeting RAB proteins and disturbing the protein trafficking pathway. Mol. Plant Pathol. 23:121721–36
    [Google Scholar]
  71. 71.
    Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M et al. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–83
    [Google Scholar]
  72. 72.
    Ma X, Claus LAN, Leslie ME, Tao K, Wu Z et al. 2020. Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581:199–203
    [Google Scholar]
  73. 73.
    Machado Wood AK, Panwar V, Grimwade-Mann M, Ashfield T, Hammond-Kosack KE, Kanyuka K 2021. The vesicular trafficking system component MIN7 is required for minimizing Fusarium graminearum infection. J. Exp. Bot. 72:5010–23
    [Google Scholar]
  74. 74.
    Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89
    [Google Scholar]
  75. 75.
    Maricchiolo E, Panfili E, Pompa A, De Marchis F, Bellucci M, Pallotta MT. 2022. Unconventional pathways of protein secretion: mammals vs. plants. Front. . Cell Dev. Biol. 10:895853
    [Google Scholar]
  76. 76.
    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]
  77. 77.
    Mei K, Guo W. 2018. The exocyst complex. Curr. Biol. 28:R922–25
    [Google Scholar]
  78. 78.
    Mei Y, Wright KM, Haegeman A, Bauters L, Diaz-Granados A et al. 2018. The Globodera pallida SPRYSEC effector Gp SPRY-414-2 that suppresses plant defenses targets a regulatory component of the dynamic microtubule network. Front. Plant Sci. 9:1019
    [Google Scholar]
  79. 79.
    Micali CO, Neumann U, Grunewald D, Panstruga R, O'Connell R. 2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell. Microbiol. 13:210–26
    [Google Scholar]
  80. 80.
    Michalopoulou VA, Mermigka G, Kotsaridis K, Mentzelopoulou A, Celie PHN et al. 2022. The host exocyst complex is targeted by a conserved bacterial type-III effector that promotes virulence. Plant Cell 34:3400–24
    [Google Scholar]
  81. 81.
    New J, Thomas SM. 2019. Autophagy-dependent secretion: mechanism, factors secreted, and disease implications. Autophagy 15:1682–93
    [Google Scholar]
  82. 82.
    Nielsen E. 2020. The small GTPase superfamily in plants: a conserved regulatory module with novel functions. Annu. Rev. Plant Biol. 71:247–72
    [Google Scholar]
  83. 83.
    Nielsen E, Cheung AY, Ueda T. 2008. The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol. 147:1516–26
    [Google Scholar]
  84. 84.
    Nielsen ME, Thordal-Christensen H. 2013. Transcytosis shuts the door for an unwanted guest. Trends Plant Sci. 18:611–16
    [Google Scholar]
  85. 85.
    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
    [Google Scholar]
  86. 86.
    Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. PNAS 108:10774–79
    [Google Scholar]
  87. 87.
    Pandey P, Leary AY, Tumtas Y, Savage Z, Dagvadorj B et al. 2021. An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface. eLife 10:e65285
    [Google Scholar]
  88. 88.
    Pecenkova T, Hala M, Kulich I, Kocourkova D, Drdova E et al. 2011. The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J. Exp. Bot. 62:2107–16
    [Google Scholar]
  89. 89.
    Petre B, Contreras MP, Bozkurt TO, Schattat MH, Sklenar J et al. 2021. Host-interactor screens of Phytophthora infestans RXLR proteins reveal vesicle trafficking as a major effector-targeted process. Plant Cell 33:1447–71
    [Google Scholar]
  90. 90.
    Ponpuak M, Mandell MA, Kimura T, Chauhan S, Cleyrat C, Deretic V. 2015. Secretory autophagy. Curr. Opin Cell Biol. 35:106–16
    [Google Scholar]
  91. 91.
    Redditt TJ, Chung EH, Karimi HZ, Rodibaugh N, Zhang Y et al. 2019. AvrRpm1 functions as an ADP-ribosyl transferase to modify NOI domain-containing proteins, including Arabidopsis and soybean RPM1-interacting protein4. Plant Cell 31:2664–81
    [Google Scholar]
  92. 92.
    Rodriguez PA, Escudero-Martinez C, Bos JI. 2017. An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence. Plant Physiol. 173:1892–903
    [Google Scholar]
  93. 93.
    Ruano G, Scheuring D. 2020. Plant cells under attack: unconventional endomembrane trafficking during plant defense. Plants 9:3389
    [Google Scholar]
  94. 94.
    Rubiato HM, Liu M, O'Connell RJ, Nielsen ME. 2022. Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens. eLife 11:e73487
    [Google Scholar]
  95. 95.
    Rutter BD, Innes RW. 2017. Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiol. 173:728–41
    [Google Scholar]
  96. 96.
    Sabol P, Kulich I, Zarsky V. 2017. RIN4 recruits the exocyst subunit EXO70B1 to the plasma membrane. J. Exp. Bot. 68:3253–65
    [Google Scholar]
  97. 97.
    Saeed B, Brillada C, Trujillo M. 2019. Dissecting the plant exocyst. Curr. Opin. Plant Biol. 52:69–76
    [Google Scholar]
  98. 98.
    Saile SC, Ackermann FM, Sunil S, Keicher J, Bayless A et al. 2021. Arabidopsis ADR1 helper NLR immune receptors localize and function at the plasma membrane in a phospholipid dependent manner. New Phytol. 232:2440–56
    [Google Scholar]
  99. 99.
    Saito C, Ueda T. 2009. Functions of RAB and SNARE proteins in plant life. Int. Rev. Cell Mol. Biol. 274:183–233
    [Google Scholar]
  100. 100.
    Savage Z, Duggan C, Toufexi A, Pandey P, Liang Y et al. 2021. Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans. Plant J. 107:1771–87
    [Google Scholar]
  101. 101.
    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]
  102. 102.
    Schulze S, Kay S, Büttner D, Egler M, Eschen-Lippold L et al. 2012. Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. New Phytol. 195:894–911
    [Google Scholar]
  103. 103.
    Solinger JA, Spang A. 2013. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J. 280:2743–57
    [Google Scholar]
  104. 104.
    Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S et al. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–24
    [Google Scholar]
  105. 105.
    Speth EB, Imboden L, Hauck P, He SY. 2009. Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol. 149:1824–37
    [Google Scholar]
  106. 106.
    Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A et al. 2006. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–46
    [Google Scholar]
  107. 107.
    Steinbrenner AD, Saldivar E, Hodges N, Guayazan-Palacios N, Chaparro AF, Schmelz EA. 2022. Signatures of plant defense response specificity mediated by herbivore-associated molecular patterns in legumes. Plant J. 110:1255–70
    [Google Scholar]
  108. 108.
    Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513–25
    [Google Scholar]
  109. 109.
    Sun H, Zhu X, Li C, Ma Z, Han X et al. 2021. Xanthomonas effector XopR hijacks host actin cytoskeleton via complex coacervation. Nat. Commun. 12:4064
    [Google Scholar]
  110. 110.
    Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M et al. 2012. N-terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Mol. Plant-Microbe Interact. 25:379–92
    [Google Scholar]
  111. 111.
    Testi S, Kuhn M-L, Allasia V, Auroy P, Kong F et al. 2019. An oomycete effector impairs autophagy in evolutionary distant organisms and favors host infection. bioRxiv 697136 . https://doi.org/10.1101/697136
    [Crossref]
  112. 112.
    Tomczynska I, Stumpe M, Mauch F. 2018. A conserved RxLR effector interacts with host RABA-type GTPases to inhibit vesicle-mediated secretion of antimicrobial proteins. Plant J. 95:187–203
    [Google Scholar]
  113. 113.
    Tsakiri D, Kotsaridis K, Michalopoulou VA, Kokkinidis M, Sarris PF. 2022. Ralstonia solanacearum core effector RipE1 interacts and cleaves the Arabidopsis exocyst component Exo70B1. bioRxiv 506019 . https://doi.org/10.1101/2022.08.31.506019
    [Crossref]
  114. 114.
    Underwood W, Somerville SC. 2008. Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59:3501–8
    [Google Scholar]
  115. 115.
    Üstün S, Hafrén A, Liu Q, Marshall RS, Minina EA et al. 2018. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell 30:668–85
    [Google Scholar]
  116. 116.
    Viotti C, Bubeck J, Stierhof YD, 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]
  117. 117.
    Wang H, Guo B, Yang B, Li H, Xu Y et al. 2021. An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection. PLOS Pathog. 17:e1010104
    [Google Scholar]
  118. 118.
    Wang J, Hu M, Wang J, Qi J, Han Z et al. 2019. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:6435eaav5870
    [Google Scholar]
  119. 119.
    Wang P, Hussey PJ. 2015. Interactions between plant endomembrane systems and the actin cytoskeleton. Front. Plant Sci. 6:422
    [Google Scholar]
  120. 120.
    Wang S, McLellan H, Bukharova T, He Q, Murphy F et al. 2019. Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization. J. Exp. Bot. 70:343–56
    [Google Scholar]
  121. 121.
    Wang W, Liu N, Gao C, Cai H, Romeis T, Tang D. 2020. The Arabidopsis exocyst subunits EXO70B1 and EXO70B2 regulate FLS2 homeostasis at the plasma membrane. New Phytol. 227:529–44
    [Google Scholar]
  122. 122.
    Wang W, Liu N, Gao C, Rui L, Tang D. 2019. The Pseudomonas syringae effector AvrPtoB associates with and ubiquitinates Arabidopsis exocyst subunit EXO70B1. Front. Plant Sci. 10:1027
    [Google Scholar]
  123. 123.
    Wang X, Chung KP, Lin W, Jiang L. 2018. Protein secretion in plants: conventional and unconventional pathways and new techniques. J. Exp. Bot. 69:21–37
    [Google Scholar]
  124. 124.
    Wawra S, Trusch F, Matena A, Apostolakis K, Linne U et al. 2017. The RxLR motif of the host targeting effector AVR3a of Phytophthora infestans is cleaved before secretion. Plant Cell 29:1184–95
    [Google Scholar]
  125. 125.
    Weaver LM, Swiderski MR, Li Y, Jones JD. 2006. The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J. 47:829–40
    [Google Scholar]
  126. 126.
    Wei T, Wang A. 2008. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 82:12252–64
    [Google Scholar]
  127. 127.
    Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–18
    [Google Scholar]
  128. 128.
    Wick P, Gansel X, Oulevey C, Page V, Studer I et al. 2003. The expression of the t-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol. 132:343–51
    [Google Scholar]
  129. 129.
    Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235–47
    [Google Scholar]
  130. 130.
    Yang M, Ismayil A, Jiang Z, Wang Y, Zheng X et al. 2022. A viral protein disrupts vacuolar acidification to facilitate virus infection in plants. EMBO J. 41:e108713
    [Google Scholar]
  131. 131.
    Yang M, Zhang Y, Xie X, Yue N, Li J et al. 2018. Barley stripe mosaic virus γb protein subverts autophagy to promote viral infection by disrupting the ATG7-ATG8 interaction. Plant Cell 30:1582–95
    [Google Scholar]
  132. 132.
    Yuan H-Y, Yao L-L, Jia Z-Q, Li Y, Li Y-Z. 2006. Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells. Protoplasma 229:75–82
    [Google Scholar]
  133. 133.
    Yun HS, Kwon C. 2017. Vesicle trafficking in plant immunity. Curr. Opin. Plant Biol. 40:34–42
    [Google Scholar]
  134. 134.
    Zhang H, Zhang L, Gao B, Fan H, Jin J et al. 2011. Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLOS ONE 6:e26477
    [Google Scholar]
  135. 135.
    Zhang Y, Liu CM, Emons AM, Ketelaar T. 2010. The plant exocyst. J. Integr. Plant Biol. 52:138–46
    [Google Scholar]
  136. 136.
    Zhang Z, Feechan A, Pedersen C, Newman MA, Qiu JL et al. 2007. A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant J. 49:302–12
    [Google Scholar]
  137. 137.
    Zhao T, Rui L, Li J, Nishimura MT, Vogel JP 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]
  138. 138.
    Zhuang X, Jiang L. 2014. Autophagosome biogenesis in plants: roles of SH3P2. Autophagy 10:704–5
    [Google Scholar]
  139. 139.
    Zvereva AS, Golyaev V, Turco S, Gubaeva EG, Rajeswaran R et al. 2016. Viral protein suppresses oxidative burst and salicylic acid-dependent autophagy and facilitates bacterial growth on virus-infected plants. New Phytol. 211:1020–34
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021622-123232
Loading
/content/journals/10.1146/annurev-phyto-021622-123232
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