1932

Abstract

Viruses, causal agents of devastating diseases in plants, are obligate intracellular pathogens composed of a nucleic acid genome and a limited number of viral proteins. The diversity of plant viruses, their diminutive molecular nature, and their symplastic localization pose challenges to understanding the interplay between these pathogens and their hosts in the currently accepted framework of plant innate immunity. It is clear, nevertheless, that plants can recognize the presence of a virus and activate antiviral immune responses, although our knowledge of the breadth of invasion signals and the underpinning sensing events is far from complete. Below, I discuss some of the demonstrated or hypothesized mechanisms enabling viral recognition in plants, the step preceding the onset of antiviral immunity, as well as the strategies viruses have evolved to evade or suppress their detection.

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2024-07-22
2025-04-26
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Literature Cited

  1. 1.
    Akhter MS, Nakahara KS, Masuta C. 2021.. Resistance induction based on the understanding of molecular interactions between plant viruses and host plants. . Virol. J. 18::176
    [Crossref] [Google Scholar]
  2. 2.
    Barbero F, Guglielmotto M, Capuzzo A, Maffei ME. 2016.. Extracellular self-DNA (esDNA), but not heterologous plant or insect DNA (etDNA), induces plasma membrane depolarization and calcium signaling in lima bean (Phaseolus lunatus) and maize (Zea mays). . Int. J. Mol. Sci. 17::1659
    [Crossref] [Google Scholar]
  3. 3.
    Barton DA, Roovers EF, Gouil Q, da Fonseca GC, Reis RS, et al. 2017.. Live cell imaging reveals the relocation of dsRNA binding proteins upon viral infection. . Mol. Plant Microbe Interact. 30::43543
    [Crossref] [Google Scholar]
  4. 4.
    Baulcombe DC. 2022.. The role of viruses in identifying and analyzing RNA silencing. . Annu. Rev. Virol. 9::35373
    [Crossref] [Google Scholar]
  5. 5.
    Belshaw R, Gardner A, Rambaut A, Pybus OG. 2008.. Pacing a small cage: mutation and RNA viruses. . Trends Ecol. Evol. 23::18893
    [Crossref] [Google Scholar]
  6. 6.
    Bentham AR, De la Concepcion JC, Mukhi N, Zdrzałek R, Draeger M, et al. 2020.. A molecular roadmap to the plant immune system. . J. Biol. Chem. 295::1491635
    [Crossref] [Google Scholar]
  7. 7.
    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::352841.e12
    [Crossref] [Google Scholar]
  8. 8.
    Bologna NG, Iselin R, Abriata LA, Sarazin A, Pumplin N, et al. 2018.. Nucleo-cytosolic shuttling of ARGONAUTE1 prompts a revised model of the plant microRNA pathway. . Mol. Cell 69::70919.e5
    [Crossref] [Google Scholar]
  9. 9.
    Brommonschenkel SH, Frary A, Frary A, Tanksley SD. 2000.. The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mol. . Plant Microbe Interact. 13::113038
    [Crossref] [Google Scholar]
  10. 10.
    Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 2007.. A novel role for the TIR domain in association with pathogen-derived elicitors. . PLOS Biol. 5::50114
    [Crossref] [Google Scholar]
  11. 11.
    Campillo-Balderas JA, Lazcano A, Becerra A. 2015.. Viral genome size distribution does not correlate with the antiquity of the host lineages. . Front. Ecol. Evol. 3::143
    [Crossref] [Google Scholar]
  12. 12.
    Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP. 2008.. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. . Cell 132::44962
    [Crossref] [Google Scholar]
  13. 13.
    Caplan JL, Zhu XH, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP. 2009.. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. . Cell Host Microbe 6::45769
    [Crossref] [Google Scholar]
  14. 14.
    Carbonell A, García JA, Simón-Mateo C, Hernández C. 2016.. Plant virus RNA replication. . eLS. https://doi.org/10.1002/9780470015902.a0022338
    [Google Scholar]
  15. 15.
    Carty M, Guy C, Bowie AG. 2021.. Detection of viral infections by innate immunity. . Biochem. Pharmacol. 183::114316
    [Crossref] [Google Scholar]
  16. 16.
    Carvalho CM, Santos AA, Pires SR, Rocha CS, Saraiva DI, et al. 2008.. Regulated nuclear trafficking of rpL10A mediated by NIK1 represents a defense strategy of plant cells against virus. . PLOS Pathog. 4::e1000247
    [Crossref] [Google Scholar]
  17. 17.
    Ceniceros-Ojeda EA, Rodríguez-Negrete EA, Rivera-Bustamante RF. 2016.. Two populations of viral minichromosomes are present in a geminivirus-infected plant showing symptom remission (recovery). . J. Virol. 90::382838
    [Crossref] [Google Scholar]
  18. 18.
    Cesari S. 2018.. Multiple strategies for pathogen perception by plant immune receptors. . New Phytol. 219::1724
    [Crossref] [Google Scholar]
  19. 19.
    Chen HY, Yang J, Lin C, Yuan YA. 2008.. Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. . EMBO Rep. 9::75460
    [Crossref] [Google Scholar]
  20. 20.
    Chen I-H, Chang J-E, Wu C-Y, Huang Y-P, Hsu Y-H, Tsai C-H. 2019.. An E3 ubiquitin ligase from Nicotiana benthamiana targets the replicase of Bamboo mosaic virus and restricts its replication. . Mol. Plant Pathol. 20::67384
    [Crossref] [Google Scholar]
  21. 21.
    Chen J, Zhao YX, Luo XJ, Hong H, Yang TQ, et al. 2023.. NLR surveillance of pathogen interference with hormone receptors induces immunity. . Nature 613::145152. Erratum . 2023.. Nature 614::E16 21. An example of NLR-mediated antiviral immunity: An NLR recognizes the viral manipulation of hormone signaling.
    [Google Scholar]
  22. 22.
    Chen TY, Liu D, Niu X, Wang J, Qian L, et al. 2017.. Antiviral resistance protein Tm-22 functions on the plasma membrane. . Plant Physiol. 173::2399410
    [Crossref] [Google Scholar]
  23. 23.
    Chiusano ML, Incerti G, Colantuono C, Termolino P, Palomba E, et al. 2021.. Arabidopsis thaliana response to extracellular DNA: self versus nonself exposure. . Plants 10::1744
    [Crossref] [Google Scholar]
  24. 24.
    Choi JJ, Klosterman SJ, Hadwiger LA. 2001.. A comparison of the effects of DNA-damaging agents and biotic elicitors on the induction of plant defense genes, nuclear distortion, and cell death. . Plant Physiol. 125::75262
    [Crossref] [Google Scholar]
  25. 25.
    Cook DE, Mesarich CH, Thomma BPHJ. 2015.. Understanding plant immunity as a surveillance system to detect invasion. . Annu. Rev. Phytopathol. 53::54163
    [Crossref] [Google Scholar]
  26. 26.
    Crespo-Bellido A, Duffy S. 2023.. The how of counter-defense: viral evolution to combat host immunity. . Curr. Opin. Microbiol. 74::102320
    [Crossref] [Google Scholar]
  27. 27.
    Csorba T, Kontra L, Burgyán J. 2015.. viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence. . Virology 479::85103
    [Crossref] [Google Scholar]
  28. 28.
    Ding SW. 2023.. Transgene silencing, RNA interference, and the antiviral defense mechanism directed by small interfering RNAs. . Phytopathology 113::61625
    [Crossref] [Google Scholar]
  29. 29.
    Dubiella U, Serrano I. 2021.. The ubiquitin proteasome system as a double agent in plant-virus interactions. . Plants 10::928
    [Crossref] [Google Scholar]
  30. 30.
    Duran-Flores D, Heil M. 2015.. Growth inhibition by self-DNA: a phenomenon and its multiple explanations. . New Phytol. 207::48285
    [Crossref] [Google Scholar]
  31. 31.
    Duxbury Z, Wu CH, Ding PT. 2021.. A comparative overview of the intracellular guardians of plants and animals: NLRs in innate immunity and beyond. . Annu. Rev. Plant Biol. 72::15584
    [Crossref] [Google Scholar]
  32. 32.
    Eamens AL, Kim KW, Curtin SJ, Waterhouse PM. 2012.. DRB2 is required for microRNA biogenesis in Arabidopsis thaliana. . PLOS ONE 7::e35933
    [Crossref] [Google Scholar]
  33. 33.
    Eamens AL, Wook Kim K, Waterhouse PM. 2012.. DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway in Arabidopsis thaliana. . Plant Signal. Behav. 7::122429
    [Crossref] [Google Scholar]
  34. 34.
    Escocard de Azevedo Manhães AM, Ortiz-Morea FA, He P, Shan LB. 2021.. Plant plasma membrane-resident receptors: surveillance for infections and coordination for growth and development. . J. Integr. Plant Biol. 63::79101
    [Crossref] [Google Scholar]
  35. 35.
    Fang Y, Spector DL. 2007.. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. . Curr. Biol. 17::81823
    [Crossref] [Google Scholar]
  36. 36.
    Fátyol K, Fekete KA, Ludman M. 2020.. Double-stranded-RNA-binding protein 2 participates in antiviral defense. . J. Virol. 94::e00017-20
    [Crossref] [Google Scholar]
  37. 37.
    Förderer A, Li E, Lawson AW, Deng Y-N, Sun Y, et al. 2022.. A wheat resistosome defines common principles of immune receptor channels. . Nature 610::53239
    [Crossref] [Google Scholar]
  38. 38.
    Ghoshal B, Sanfacon H. 2014.. Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with tomato ringspot virus is associated with reduced translation of viral RNA2 and requires ARGONAUTE 1. . Virology 456::18897
    [Crossref] [Google Scholar]
  39. 39.
    Gong P, Tan H, Zhao S, Li H, Liu H, et al. 2021.. Geminiviruses encode additional small proteins with specific subcellular localizations and virulence function. . Nat. Commun. 12::4278
    [Crossref] [Google Scholar]
  40. 40.
    Guzmán-Benito I, Donaire L, Amorim-Silva V, Vallarino JG, Esteban A, et al. 2019.. The immune repressor BIR1 contributes to antiviral defense and undergoes transcriptional and post-transcriptional regulation during viral infections. . New Phytol. 224::42138
    [Crossref] [Google Scholar]
  41. 41.
    Hadwiger LA, Tanaka K. 2017.. Non-host resistance: DNA damage is associated with SA signaling for induction of PR genes and contributes to the growth suppression of a pea pathogen on pea endocarp tissue. . Front. Plant Sci. 8::446
    [Crossref] [Google Scholar]
  42. 42.
    Hafrén A, Hofius D. 2017.. NBR1-mediated antiviral xenophagy in plant immunity. . Autophagy 13::20001
    [Crossref] [Google Scholar]
  43. 43.
    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::E202635 43. Together with Reference 46, this article provides the first proof of autophagy as a plant antiviral mechanism.
    [Crossref] [Google Scholar]
  44. 44.
    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::64962
    [Crossref] [Google Scholar]
  45. 45.
    Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. 2013.. Geminiviruses: masters at redirecting and reprogramming plant processes. . Nat. Rev. Microbiol. 11::77788
    [Crossref] [Google Scholar]
  46. 46.
    Haxim Y, Ismayil A, Jia Q, Wang Y, Zheng X, et al. 2017.. Autophagy functions as an antiviral mechanism against geminiviruses in plants. . eLife 6:e23897 46. Together with Reference 43, this article provides the first proof of autophagy as a plant antiviral mechanism.
    [Google Scholar]
  47. 47.
    Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, et al. 2005.. Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. . Plant Mol. Biol. 57::17388
    [Crossref] [Google Scholar]
  48. 48.
    Ho JSY, Zhu Z, Marazzi I. 2021.. Unconventional viral gene expression mechanisms as therapeutic targets. . Nature 593::36271
    [Crossref] [Google Scholar]
  49. 49.
    Hoffmann G, López-González S, Mahboubi A, Hanson J, Hafrén A. 2023.. Cauliflower mosaic virus protein P6 is a multivalent node for RNA granule proteins and interferes with stress granule responses during plant infection. . Plant Cell 35::336382
    [Crossref] [Google Scholar]
  50. 50.
    Horsefield S, Burdett H, Zhang X, Manik MK, Shi Y, et al. 2019.. NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. . Science 365::79399
    [Crossref] [Google Scholar]
  51. 51.
    Hu ZH, Chai JJ. 2023.. Assembly and architecture of NLR resistosomes and inflammasomes. . Annu. Rev. Biophys. 52::20728
    [Crossref] [Google Scholar]
  52. 52.
    Huang C, Sede AR, Elvira-González L, Yan Y, Rodriguez ME, et al. 2023.. dsRNA-induced immunity targets plasmodesmata and is suppressed by viral movement proteins. . Plant Cell 35::384569 52. This article shows that dsRNA/poly(I:C) treatment promotes callose deposition at plasmodesmata, limiting viral movement.
    [Crossref] [Google Scholar]
  53. 53.
    Huang CJ. 2021.. From player to pawn: viral avirulence factors involved in plant immunity. . Viruses 13::688
    [Crossref] [Google Scholar]
  54. 54.
    Huang SJ, Jia AL, Song W, Hessler G, Meng YG, et al. 2022.. Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity. . Science 377::eabq3297
    [Crossref] [Google Scholar]
  55. 55.
    Hung Y-H, Slotkin RK. 2021.. The initiation of RNA interference (RNAi) in plants. . Curr. Opin. Plant Biol. 61::102014
    [Crossref] [Google Scholar]
  56. 56.
    Incarbone M, Clavel M, Monsion B, Kuhn L, Scheer H, et al. 2021.. Immunocapture of dsRNA-bound proteins provides insight into Tobacco rattle virus replication complexes and reveals Arabidopsis DRB2 to be a wide-spectrum antiviral effector. . Plant Cell 33::340220
    [Crossref] [Google Scholar]
  57. 57.
    Incarbone M, Zimmermann A, Hammann P, Erhardt M, Michel F, Dunoyer P. 2017.. Neutralization of mobile antiviral small RNA through peroxisomal import. . Nat. Plants 3::17094 57. A beautiful example of VSR activity through binding and organellar confinement of siRNA.
    [Crossref] [Google Scholar]
  58. 58.
    Iwasaki A. 2012.. A virological view of innate immune recognition. . Annu. Rev. Microbiol. 66::17796
    [Crossref] [Google Scholar]
  59. 59.
    Jacob P, Kim NH, Wu F, El-Kasmi F, Chi Y, et al. 2021.. Plant “helper” immune receptors are Ca2+-permeable nonselective cation channels. . Science 373::42025
    [Crossref] [Google Scholar]
  60. 60.
    Jia A, Huang S, Song W, Wang J, Meng Y, et al. 2022.. TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity. . Science 377::eabq8180
    [Crossref] [Google Scholar]
  61. 61.
    Jiang L, Lu Y, Zheng X, Yang X, Chen Y, et al. 2021.. The plant protein NbP3IP directs degradation of Rice stripe virus p3 silencing suppressor protein to limit virus infection through interaction with the autophagy-related protein NbATG8. . New Phytol. 229::103651
    [Crossref] [Google Scholar]
  62. 62.
    Jin Y, Zhao JH, Guo HS. 2021.. Recent advances in understanding plant antiviral RNAi and viral suppressors of RNAi. . Curr. Opin. Virol. 46::6572
    [Crossref] [Google Scholar]
  63. 63.
    Jones RAC. 2021.. Global plant virus disease pandemics and epidemics. . Plants 10::233
    [Crossref] [Google Scholar]
  64. 64.
    Jouannet V, Moreno AB, Elmayan T, Vaucheret H, Crespi MD, Maizel A. 2012.. Cytoplasmic Arabi-dopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. . EMBO J. 31::170413
    [Crossref] [Google Scholar]
  65. 65.
    Kong J, Wei M, Li G, Lei R, Qiu Y, et al. 2018.. The cucumber mosaic virus movement protein suppresses PAMP-triggered immune responses in Arabidopsis and tobacco. . Biochem. Biophys. Res. Commun. 498::395401
    [Crossref] [Google Scholar]
  66. 66.
    Koonin EV, Krupovic M, Agol VI. 2021.. The Baltimore classification of viruses 50 years later: How does it stand in the light of virus evolution?. Microbiol. Mol. Biol. Rev. 85::e0005321
    [Crossref] [Google Scholar]
  67. 67.
    Korner CJ, Klauser D, Niehl A, Dominguez-Ferreras A, Chinchilla D, et al. 2013.. The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. . Mol. Plant Microbe Interact. 26::127180 67. An early example of an RLK, BAK1, as a contributor to antiviral resistance in plants.
    [Crossref] [Google Scholar]
  68. 68.
    Kørner CJ, Pitzalis N, Peña EJ, Erhardt M, Vazquez F, Heinlein M. 2018.. Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. . Nat. Plants 4::15764
    [Crossref] [Google Scholar]
  69. 69.
    Krupovič M, Bamford DH. 2008.. Virus evolution: How far does the double β-barrel viral lineage extend?. Nat. Rev. Microbiol. 6::94148
    [Crossref] [Google Scholar]
  70. 70.
    Kushwaha NK, Hafrén A, Hofius D. 2019.. Autophagy–virus interplay in plants: from antiviral recognition to proviral manipulation. . Mol. Plant Pathol. 20::121116
    [Crossref] [Google Scholar]
  71. 71.
    Langin G, González-Fuente M, Üstün S. 2023.. The plant ubiquitin–proteasome system as a target for microbial manipulation. . Annu. Rev. Phytopathol. 61::35173
    [Crossref] [Google Scholar]
  72. 72.
    Lee B, Park Y-S, Lee S, Song GC, Ryu C-M. 2016.. Bacterial RNAs activate innate immunity in Arabidopsis. . New Phytol. 209::78597
    [Crossref] [Google Scholar]
  73. 73.
    Li CF, Henderson IR, Song L, Fedoroff N, Lagrange T, Jacobsen SE. 2008.. Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. . PLOS Genet. 4::e27
    [Crossref] [Google Scholar]
  74. 74.
    Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, et al. 2006.. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. . Cell 126::93106
    [Crossref] [Google Scholar]
  75. 75.
    Li F, Zhang C, Li Y, Wu G, Hou X, et al. 2018.. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. . Nat. Commun. 9::1268
    [Crossref] [Google Scholar]
  76. 76.
    Li F, Zhang M, Zhang C, Zhou X. 2020.. Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants. . New Phytol. 225::174661
    [Crossref] [Google Scholar]
  77. 77.
    Li HW, Lucy AP, Guo HS, Li WX, Ji LH, et al. 1999.. Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. . EMBO J. 18::268391
    [Crossref] [Google Scholar]
  78. 78.
    Li J, Huang HN, Zhu M, Huang S, Zhang WH, et al. 2019.. A plant immune receptor adopts a two-step recognition mechanism to enhance viral effector perception. . Mol. Plant 12::24862
    [Crossref] [Google Scholar]
  79. 79.
    Li Q, Wang C, Mou Z. 2020.. Perception of damaged self in plants. . Plant Physiol. 182::154565
    [Crossref] [Google Scholar]
  80. 80.
    Lind NA, Rael VE, Pestal K, Liu B, Barton GM. 2022.. Regulation of the nucleic acid-sensing Toll-like receptors. . Nat. Rev. Immunol. 22::22435
    [Crossref] [Google Scholar]
  81. 81.
    Liu H, Chang Z, Zhao S, Gong P, Zhang M, et al. 2023.. Functional identification of a novel C7 protein of tomato yellow leaf curl virus. . Virology 585::11726
    [Crossref] [Google Scholar]
  82. 82.
    Lopez-Gomollon S, Baulcombe DC. 2022.. Roles of RNA silencing in viral and non-viral plant immunity and in the crosstalk between disease resistance systems. . Nat. Rev. Mol. Cell Bio. 23::64562
    [Crossref] [Google Scholar]
  83. 83.
    Luna AP, Morilla G, Voinnet O, Bejarano ER. 2012.. Functional analysis of gene-silencing suppressors from tomato yellow leaf curl disease viruses. . Mol. Plant Microbe Interact. 25::1294306
    [Crossref] [Google Scholar]
  84. 84.
    Ma S, Lapin D, Liu L, Sun Y, Song W, et al. 2020.. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. . Science 370::eabe3069
    [Crossref] [Google Scholar]
  85. 85.
    Ma Z, Ni G, Damania B. 2018.. Innate sensing of DNA virus genomes. . Annu. Rev. Virol. 5::34162
    [Crossref] [Google Scholar]
  86. 86.
    Manghwar H, Li J. 2022.. Endoplasmic reticulum stress and unfolded protein response signaling in plants. . Int. J. Mol. Sci. 23::828
    [Crossref] [Google Scholar]
  87. 87.
    Martin R, Qi TC, Zhang HB, Liu FR, King M, et al. 2020.. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. . Science 370::eabd9993
    [Crossref] [Google Scholar]
  88. 88.
    Mazzoleni S, Carteni F, Bonanomi G, Senatore M, Termolino P, et al. 2015.. Inhibitory effects of extracellular self-DNA: a general biological process?. New Phytol. 206::12732
    [Crossref] [Google Scholar]
  89. 89.
    Medina-Puche L, Lozano-Duran R. 2019.. Tailoring the cell: a glimpse of how plant viruses manipulate their hosts. . Curr. Opin. Plant Biol. 52::16473
    [Crossref] [Google Scholar]
  90. 90.
    Medina-Puche L, Tan H, Dogra V, Wu MS, Rosas-Diaz T, et al. 2020.. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. . Cell 182::110924.e25
    [Crossref] [Google Scholar]
  91. 91.
    Meier N, Hatch C, Nagalakshmi U, Dinesh-Kumar SP. 2019.. Perspectives on intracellular perception of plant viruses. . Mol. Plant Pathol. 20::118590
    [Crossref] [Google Scholar]
  92. 92.
    Movahed N, Cabanillas DG, Wan J, Vali H, Laliberté JF, Zheng H. 2019.. Turnip mosaic virus components are released into the extracellular space by vesicles in infected leaves. . Plant Physiol. 180::137588
    [Crossref] [Google Scholar]
  93. 93.
    Nakahara KS, Masuta C, Yamada S, Shimura H, Kashihara Y, et al. 2012.. Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. . PNAS 109::1011318
    [Crossref] [Google Scholar]
  94. 94.
    Ngou BPM, Ahn H-K, Ding P, Jones JDG. 2021.. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. . Nature 592::11015
    [Crossref] [Google Scholar]
  95. 95.
    Nicaise V, Candresse T. 2017.. Plum pox virus capsid protein suppresses plant pathogen-associated molecular pattern (PAMP)-triggered immunity. . Mol. Plant Pathol. 18::87886 95. An early example of a plant virus-encoded protein with the ability to suppress PTI readouts.
    [Crossref] [Google Scholar]
  96. 96.
    Niehl A, Wyrsch I, Boller T, Heinlein M. 2016.. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. . New Phytol. 211::100819
    [Crossref] [Google Scholar]
  97. 97.
    Palukaitis P, Yoon J-Y. 2020.. R gene mediated defense against viruses.. Curr. Opin. Virol. 45::17. Erratum . 2020.. Curr. Opin. Virol. 42::65
    [Google Scholar]
  98. 98.
    Paudel DB, Sanfacon H. 2018.. Exploring the diversity of mechanisms associated with plant tolerance to virus infection. . Front. Plant Sci. 9::1575
    [Crossref] [Google Scholar]
  99. 99.
    Piedra-Aguilera A, Jiao C, Luna AP, Villanueva F, Dabad M, et al. 2019.. Integrated single-base resolution maps of transcriptome, sRNAome and methylome of Tomato yellow leaf curl virus (TYLCV) in tomato. . Sci. Rep. 9::2863
    [Crossref] [Google Scholar]
  100. 100.
    Pruitt RN, Locci F, Wanke F, Zhang LS, Saile SC, et al. 2021.. The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. . Nature 598::49599
    [Crossref] [Google Scholar]
  101. 101.
    Ristaino JB, Anderson PK, Bebber DP, Brauman KA, Cunniffe NJ, et al. 2021.. The persistent threat of emerging plant disease pandemics to global food security. . PNAS 118::e2022239118. Erratum . 2021.. PNAS 118::e2115792118
    [Google Scholar]
  102. 102.
    Sansregret R, Dufour V, Langlois M, Daayf F, Dunoyer P, et al. 2013.. Extreme resistance as a host counter-counter defense against viral suppression of RNA silencing. . PLOS Pathog. 9::e1003435
    [Crossref] [Google Scholar]
  103. 103.
    Schulze S, Yu L, Hua C, Zhang LS, Kolb D, et al. 2022.. The Arabidopsis TIR-NBS-LRR protein CSA1 guards BAK1-BIR3 homeostasis and mediates convergence of pattern- and effector-induced immune responses. . Cell Host Microbe 30::171731.e6
    [Crossref] [Google Scholar]
  104. 104.
    Shen Q, Hu T, Bao M, Cao L, Zhang H, et al. 2016.. Tobacco RING E3 ligase NtRFP1 mediates ubiquitination and proteasomal degradation of a geminivirus-encoded βC1. . Mol. Plant 9::91125
    [Crossref] [Google Scholar]
  105. 105.
    Teixeira RM, Ferreira MA, Raimundo GAS, Loriato VAP, Reis PAB, Fontes EPB. 2019.. Virus perception at the cell surface: revisiting the roles of receptor-like kinases as viral pattern recognition receptors. . Mol. Plant Pathol. 20::1196202
    [Crossref] [Google Scholar]
  106. 106.
    Toum L, Conti G, Guerriero FC, Conforte VP, Garolla FA, et al. 2020.. Single-stranded oligodeoxynucleotides induce plant defence in Arabidopsis thaliana. . Ann. Bot. 126::41322
    [Crossref] [Google Scholar]
  107. 107.
    Vega-Muñoz I, Feregrino-Pérez AA, Torres-Pacheco I, Guevara-González RG. 2018.. Exogenous fragmented DNA acts as a damage-associated molecular pattern (DAMP) inducing changes in CpG DNA methylation and defence-related responses in Lactuca sativa. . Funct. Plant Biol. 45::106572
    [Crossref] [Google Scholar]
  108. 108.
    Vega-Muñoz I, Herrera-Estrella A, Martínez-de la Vega O, Heil M. 2023.. ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response. . Front. Immunol. 14::1175786
    [Crossref] [Google Scholar]
  109. 109.
    Verchot J, Pajerowska-Mukhtar KM. 2021.. UPR signaling at the nexus of plant viral, bacterial, and fungal defenses. . Curr. Opin. Virol. 47::917
    [Crossref] [Google Scholar]
  110. 110.
    Wan J, Cabanillas DG, Zheng H, Laliberté JF. 2015.. Turnip mosaic virus moves systemically through both phloem and xylem as membrane-associated complexes. . Plant Physiol. 167::137488
    [Crossref] [Google Scholar]
  111. 111.
    Wan L, Essuman K, Anderson RG, Sasaki Y, Monteiro F, et al. 2019.. TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. . Science 365::799803
    [Crossref] [Google Scholar]
  112. 112.
    Wang JZ, Hu MJ, Wang J, Qi JF, Han ZF, et al. 2019.. Reconstitution and structure of a plant NLR resistosome conferring immunity. . Science 364::eaav5870
    [Crossref] [Google Scholar]
  113. 113.
    Wang JZ, Wang J, Hu MJ, Wu S, Qi JF, et al. 2019.. Ligand-triggered allosteric ADP release primes a plant NLR complex. . Science 364::eaav5868
    [Crossref] [Google Scholar]
  114. 114.
    Wang L, Ding Y, He L, Zhang G, Zhu JK, Lozano-Duran R. 2020.. A virus-encoded protein suppresses methylation of the viral genome through its interaction with AGO4 in the Cajal body. . eLife 9::e55542
    [Crossref] [Google Scholar]
  115. 115.
    Weber F. 2021.. Antiviral innate immunity: introduction. . In Encyclopedia of Virology, ed. DH Bamford, M Zuckerman , pp. 57783. , 4th ed..
    [Google Scholar]
  116. 116.
    Weitzman MD, Fradet-Turcotte A. 2018.. Virus DNA replication and the host DNA damage response. . Annu. Rev. Virol. 5::14164
    [Crossref] [Google Scholar]
  117. 117.
    Whitham S, Dineshkumar SP, Choi D, Hehl R, Corr C, Baker B. 1994.. The product of the tobacco mosaic-virus resistance gene N: similarity to Toll and the interleukin-1 receptor. . Cell 78::110115
    [Crossref] [Google Scholar]
  118. 118.
    Wu W, Luo X, Ren M. 2022.. Clearance or hijack: universal interplay mechanisms between viruses and host autophagy from plants to animals. . Front. Cell Infect. Microbiol. 11::786348
    [Crossref] [Google Scholar]
  119. 119.
    Wu X, Valli A, García JA, Zhou XP, Cheng XF. 2019.. The tug-of-war between plants and viruses: great progress and many remaining questions. . Viruses 11::203
    [Crossref] [Google Scholar]
  120. 120.
    Yakushiji S, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2009.. Bacterial DNA activates immunity in Arabidopsis thaliana. . J. Gen. Plant Pathol. 75::22734
    [Crossref] [Google Scholar]
  121. 121.
    Yang H, Gou XP, He K, Xi DH, Du JB, et al. 2010.. BAK1 and BKK1 in Arabidopsis thaliana confer reduced susceptibility to turnip crinkle virus. . Eur. J. Plant Pathol. 127::14956
    [Crossref] [Google Scholar]
  122. 122.
    Yang M, Ismayil A, Liu YL. 2020.. Autophagy in plant-virus interactions. . Annu. Rev. Virol. 7::40319
    [Crossref] [Google Scholar]
  123. 123.
    Ye R, Wang W, Iki T, Liu C, Wu Y, et al. 2012.. Cytoplasmic assembly and selective nuclear import of Arabidopsis ARGONAUTE4/siRNA complexes. . Mol. Cell 46::85970
    [Crossref] [Google Scholar]
  124. 124.
    Yin J, Wang L, Jin T, Nie Y, Liu H, et al. 2021.. A cell wall-localized NLR confers resistance to Soybean mosaic virus by recognizing viral-encoded cylindrical inclusion protein. . Mol. Plant 14::1881900
    [Crossref] [Google Scholar]
  125. 125.
    Yu DL, Song W, Tan EYJ, Liu L, Cao Y, et al. 2022.. TIR domains of plant immune receptors are 2′,3′-cAMP/cGMP synthetases mediating cell death. . Cell 185::237086.E18
    [Crossref] [Google Scholar]
  126. 126.
    Yuan M, Jiang Z, Bi G, Nomura K, Liu M, et al. 2021.. Pattern-recognition receptors are required for NLR-mediated plant immunity. . Nature 592::1059
    [Crossref] [Google Scholar]
  127. 127.
    Zeng RX, Liu XS, Li HY, Wu S, Huang W, et al. 2020.. Danger peptide signaling enhances internalization of a geminivirus symptom determinant in plant cells during infection. . J. Exp. Bot. 71::281727
    [Crossref] [Google Scholar]
  128. 128.
    Zhang T, Tamman H, ’t Wallant KC, Kurata T, LeRoux M, et al. 2022.. Direct activation of a bacterial innate immune system by a viral capsid protein. . Nature 612::13240
    [Crossref] [Google Scholar]
  129. 129.
    Zhao L, Rosario K, Breitbart M, Duffy S. 2019.. Eukaryotic circular Rep-encoding single-stranded DNA (CRESS DNA) viruses: ubiquitous viruses with small genomes and a diverse host range. . Adv. Virus Res. 103::71133
    [Crossref] [Google Scholar]
  130. 130.
    Zhao S, Gong P, Ren Y, Liu H, Li H, et al. 2022.. The novel C5 protein from tomato yellow leaf curl virus is a virulence factor and a suppressor of gene silencing. . Stress Biol. 2::19
    [Crossref] [Google Scholar]
  131. 131.
    Zhou X, Gao H, Zhang X, Rahman MKU, Mazzoleni S, et al. 2023.. Plant extracellular self-DNA inhibits growth and induces immunity via the jasmonate signaling pathway. . Plant Physiol. 192::247591
    [Crossref] [Google Scholar]
  132. 132.
    Zorzatto C, Machado JPB, Lopes KVG, Nascimento KJT, Pereira WA, et al. 2015.. NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. . Nature 520::67982 132. This article unveils global translation suppression as an antiviral mechanism in plants.
    [Crossref] [Google Scholar]
  133. 133.
    Zrachya A, Glick E, Levy Y, Arazi T, Citovsky V, Gafni Y. 2007.. Suppressor of RNA silencing encoded by Tomato yellow leaf curl virus-Israel. . Virology 358::15965
    [Crossref] [Google Scholar]
  134. 134.
    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::102034
    [Crossref] [Google Scholar]
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