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  • Review Article
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Evasion of plant immunity by microbial pathogens

Nature Reviews Microbiology volume 20, pages 449–464 (2022)Cite this article

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Abstract

Plant pathogenic viruses, bacteria, fungi and oomycetes cause destructive diseases in natural habitats and agricultural settings, thereby threatening plant biodiversity and global food security. The capability of plants to sense and respond to microbial infection determines the outcome of plant–microorganism interactions. Host-adapted microbial pathogens exploit various infection strategies to evade or counter plant immunity and eventually establish a replicative niche. Evasion of plant immunity through dampening host recognition or the subsequent immune signalling and defence execution is a crucial infection strategy used by different microbial pathogens to cause diseases, underpinning a substantial obstacle for efficient deployment of host genetic resistance genes for sustainable disease control. In this Review, we discuss current knowledge of the varied strategies microbial pathogens use to evade the complicated network of plant immunity for successful infection. In addition, we discuss how to exploit this knowledge to engineer crop resistance.

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Fig. 1: Stepwise activation of plant innate immunity.
Fig. 2: Microbial pathogens possess multiple mechanisms to evade plant PRR-mediated recognition.
Fig. 3: Microbial evasion of host NLR receptor-mediated recognition.
Fig. 4: Manipulation of plant immune signalling.
Fig. 5: Manipulation of plant immune output.

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References

  1. Zhou, J.-M. & Zhang, Y. Plant immunity: danger perception and signaling. Cell 181, 978–989 (2020).

    CAS  PubMed  Google Scholar 

  2. Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).

    CAS  PubMed  Google Scholar 

  3. Saile, S. C. et al. Two unequally redundant “helper” immune receptor families mediate Arabidopsis thaliana intracellular “sensor” immune receptor functions. PLoS Biol. 18, e3000783 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Wu, C.-H. et al. NLR network mediates immunity to diverse plant pathogens. Proc. Natl Acad. Sci. USA 114, 8113–8118 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Jacob, P. et al. Plant “helper” immune receptors are Ca2+-permeable nonselective cation channels. Science 373, 420–425 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bi, G. et al. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184, 3528–3541 (2021).

    CAS  PubMed  Google Scholar 

  7. Ma, S. et al. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370, eabe3069 (2020).

    CAS  PubMed  Google Scholar 

  8. Martin, R. et al. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370, eabd9993 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang, J. et al. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, eaav5870 (2019).

    CAS  PubMed  Google Scholar 

  10. Ngou, B. P. M., Ahn, H.-K., Ding, P. & Jones, J. D. G. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110–115 (2021).

    CAS  PubMed  Google Scholar 

  11. Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Pruitt, R. N. et al. The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 598, 495–499 (2021).

    CAS  PubMed  Google Scholar 

  13. Tian, H. et al. Activation of TIR signalling boosts pattern-triggered immunity. Nature 598, 500–503 (2021).

    CAS  PubMed  Google Scholar 

  14. Gomez-Gomez, L. & Boller, T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003–1011 (2000).

    CAS  PubMed  Google Scholar 

  15. Cao, Y. et al. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3, e03766 (2014).

    PubMed Central  Google Scholar 

  16. Wei, Y. et al. An immune receptor complex evolved in soybean to perceive a polymorphic bacterial flagellin. Nat. Commun. 11, 3763 (2020). This article describes a polymorphic version of FLS2 in soybean, which is capable of perceiving an flg22 variant derived from R. solanacearum.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bao, Z., Wei, H.-L., Ma, X. & Swingle, B. Pseudomonas syringae AlgU downregulates flagellin gene expression, helping evade plant immunity. J. Bacteriol. 202, e00418–e00419 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Pel, M. J. C. et al. Pseudomonas syringae evades host immunity by degrading flagellin monomers with alkaline protease AprA. Mol. Plant Microbe Interact. 27, 603–610 (2014).

    CAS  PubMed  Google Scholar 

  19. Buscaill, P. et al. Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides. Science 364, eaav0748 (2019).

    CAS  PubMed  Google Scholar 

  20. Jashni, M. K. et al. Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Mol. Plant Microbe Interact. 28, 996–1008 (2015).

    CAS  PubMed  Google Scholar 

  21. van den Burg, H. A., Harrison, S. J., Joosten, M. H. A. J., Vervoort, J. & de Wit, P. J. G. M. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe Interact. 19, 1420–1430 (2006).

    PubMed  Google Scholar 

  22. Jonge, R. D. et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953–955 (2010).

    PubMed  Google Scholar 

  23. Gao, F. et al. Deacetylation of chitin oligomers increases virulence in soil-borne fungal pathogens. Nat. Plants 5, 1167–1176 (2019).

    CAS  PubMed  Google Scholar 

  24. Martinez-Cruz, J. et al. Effectors with chitinase activity (EWCAs), a family of conserved, secreted fungal chitinases that suppress chitin-triggered immunity. Plant Cell 33, 1319–1340 (2021).

    Google Scholar 

  25. Buscaill, P. & van der Hoorn, R. A. L. Defeated by the nines: nine extracellular strategies to avoid microbe-associated molecular patterns recognition in plants. Plant Cell 33, 2116–2130 (2021).

    PubMed  PubMed Central  Google Scholar 

  26. Nicaise, V. et al. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32, 701–712 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Goehre, V. et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824–1832 (2008).

    CAS  Google Scholar 

  28. Macho, A. P. et al. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343, 1509–1512 (2014). This article shows that P. syringae evades host detection by secreting a tyrosine phosphatase to block the activation of the PRR EFR.

    CAS  PubMed  Google Scholar 

  29. Cui, H., Tsuda, K. & Parker, J. E. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487–511 (2015).

    CAS  PubMed  Google Scholar 

  30. Arnold, D. L. & Jackson, R. W. Bacterial genomes: evolution of pathogenicity. Curr. Opin. Plant Biol. 14, 385–391 (2011).

    CAS  PubMed  Google Scholar 

  31. Raffaele, S. & Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10, 417–430 (2012).

    CAS  PubMed  Google Scholar 

  32. Rouxel, T. & Balesdent, M.-H. Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. N. Phytol. 214, 526–532 (2017).

    CAS  Google Scholar 

  33. Raffaele, S. et al. Genome evolution following host jumps in the Irish Potato Famine pathogen lineage. Science 330, 1540–1543 (2010).

    CAS  PubMed  Google Scholar 

  34. Grandaubert, J. et al. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 15, 891 (2014).

    PubMed  PubMed Central  Google Scholar 

  35. Plissonneau, C. et al. A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. N. Phytol. 209, 1613–1624 (2016).

    CAS  Google Scholar 

  36. Gout, L. et al. Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ. Microbiol. 9, 2978–2992 (2007).

    CAS  PubMed  Google Scholar 

  37. Zhou, E., Jia, Y., Singh, P., Correll, J. C. & Lee, F. N. Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet. Biol. 44, 1024–1034 (2007).

    CAS  PubMed  Google Scholar 

  38. Van de Wouw, A. P. et al. Evolution of linked virulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog. 6, e1001180 (2010).

    PubMed  PubMed Central  Google Scholar 

  39. Chou, S. et al. Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc. Natl Acad. Sci. USA 108, 13323–13328 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Asai, S. et al. A downy mildew effector evades recognition by polymorphism of expression and subcellular localization. Nat. Commun. 9, 5192 (2018). This article reports that H. arabidopsidis evades the host resistance gene RPP4 through effector polymorphisms, which alter effector gene expression or effector subcellular localization.

    PubMed  PubMed Central  Google Scholar 

  41. Huang, J. et al. Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c. N. Phytol. 221, 1010–1022 (2019).

    CAS  Google Scholar 

  42. Saunders, D. G. O. et al. Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the Solanum demissum immune receptor R2 to mediate disease resistance. Plant Cell 24, 3420–3434 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Gilroy, E. M. et al. Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. N. Phytol. 191, 763–776 (2011).

    CAS  Google Scholar 

  44. Kang, S., Lebrun, M. H., Farrall, L. & Valent, B. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol. Plant Microbe Interact. 14, 671–674 (2001).

    CAS  PubMed  Google Scholar 

  45. Dong, S. et al. Sequence variants of the Phytophthora sojae RXLR effector Avr3a/5 are differentially recognized by Rps3a and Rps5 in soybean. PLoS ONE 6, e20172 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Qutob, D., Chapman, B. P. & Gijzen, M. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4, 1349–1349 (2013).

    PubMed  Google Scholar 

  47. Qutob, D. et al. Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS ONE 4, e5066 (2009).

    PubMed  PubMed Central  Google Scholar 

  48. Wang, L. et al. Effector gene silencing mediated by histone methylation underpins host adaptation in an oomycete plant pathogen. Nucleic Acids Res. 48, 1790–1799 (2020). This article reports that P. sojae evades the resistance gene Rps1b through silencing the effector gene Avr1b via histone methylation.

    CAS  PubMed  Google Scholar 

  49. Lee, J. et al. Acetylation of an NB-LRR plant immune-effector complex suppresses immunity. Cell Rep. 13, 1670–1682 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Ji, Z. et al. Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat. Commun. 7, 13435 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Champouret, N. et al. Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol. Plant Microbe Interact. 22, 1535–1545 (2009).

    CAS  PubMed  Google Scholar 

  52. Zhao, J. & Song, J. NLR immune receptor RB is differentially targeted by two homologous but functionally distinct effector proteins. Plant Commun. 2, 100236 (2021). This article reports that P. infestans evolved an epistatic effector, IPI-O4, to suppress the immune receptor RB activation by the avirulence effector IPI-O1.

    PubMed  PubMed Central  Google Scholar 

  53. Chen, Y., Liu, Z. & Halterman, D. A. Molecular determinants of resistance activation and suppression by Phytophthora infestans effector IPI-O. PLoS Pathog. 8, e1002595 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Lazar, N. et al. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins. Preprint at bioRxiv https://doi.org/10.1101/2020.12.17.423041 (2021).

    Article  Google Scholar 

  55. van der Hoorn, R. A. L. & Kamoun, S. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009–2017 (2008).

    PubMed  PubMed Central  Google Scholar 

  56. Deslandes, L. & Rivas, S. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644–655 (2012).

    CAS  PubMed  Google Scholar 

  57. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. & Dangl, J. L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389 (2003). This article reports that the P. syringae effector AvrRpt2 cleaves the guardee RIN4, which activates the matching immune receptor RPS2.

    CAS  PubMed  Google Scholar 

  58. Wilton, M. et al. The type III effector HopF2(Pto) targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc. Natl Acad. Sci. USA 107, 2349–2354 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Chung, E.-H. et al. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9, 125–136 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Kim, H.-S. et al. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl Acad. Sci. USA 102, 6496–6501 (2005). This article reports that P. syringae effector AvrRpt2-dependent cleavage and the subsequent elimination of the guardee RIN4 from the plasma membrane prevents AvrRpm1-dependent or AvrB-dependent activation of RPM1.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Rufián, J. S. et al. Suppression of HopZ effector-triggered plant immunity in a natural pathosystem. Front. Plant Sci. 9, 977 (2018).

    PubMed  PubMed Central  Google Scholar 

  62. Houterman, P. M., Cornelissen, B. J. C. & Rep, M. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog. 4, e1000061 (2008).

    PubMed  PubMed Central  Google Scholar 

  63. Derevnina, L. et al. Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. PLoS Biol. 19, e3001136 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Ma, X., Xu, G., He, P. & Shan, L. SERKing coreceptors for receptors. Trends Plant Sci. 21, 1017–1033 (2016).

    CAS  PubMed  Google Scholar 

  65. Shan, L. et al. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17–27 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Li, L. et al. Activation-dependent destruction of a co-receptor by a Pseudomonas syringae effector dampens plant immunity. Cell Host Microbe 20, 504–514 (2016). This article demonstrates that the P. syringae effector HopB1 cleaves immunoactivated BAK1 to block activation of PTI.

    CAS  PubMed  Google Scholar 

  67. Ma, X. et al. Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581, 199–203 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Feng, F. et al. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485, 114–118 (2012).

    CAS  PubMed  Google Scholar 

  69. Zhang, J. et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7, 290–301 (2010).

    CAS  PubMed  Google Scholar 

  70. Derkacheva, M. et al. The Arabidopsis E3 ubiquitin ligase PUB4 regulates BIK1 homeostasis and is targeted by a bacterial type-III effector. Preprint at bioRxiv https://doi.org/10.1101/2020.10.25.354514 (2020).

    Article  Google Scholar 

  71. Irieda, H. et al. Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases. Proc. Natl Acad. Sci. USA 116, 496–505 (2019).

    CAS  PubMed  Google Scholar 

  72. Yu, G. et al. A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity. PLoS Pathog. 16, e1008933 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Kadota, Y. & Shirasu, K. The HSP90 complex of plants. Biochim. Biophys. Acta 1823, 689–697 (2012).

    CAS  PubMed  Google Scholar 

  74. Lopez, V. A. et al. A bacterial effector mimics a host HSP90 client to undermine immunity. Cell 179, 205–218 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Dongus, J. A. & Parker, J. E. EDS1 signalling: at the nexus of intracellular and surface receptor immunity. Curr. Opin. Plant Biol. 62, 102039 (2021).

    CAS  PubMed  Google Scholar 

  76. Li, Q. et al. A Phytophthora capsici effector suppresses plant immunity via interaction with EDS1. Mol. Plant Pathol. 21, 502–511 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Zhang, J. et al. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-Induced immunity in plants. Cell Host Microbe 1, 175–185 (2007).

    CAS  PubMed  Google Scholar 

  78. Wang, Y. et al. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22, 2033–2044 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Cui, H. et al. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP Kinase 4. Cell Host Microbe 7, 164–175 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Murphy, F. et al. The potato MAP3K StVIK is required for the Phytophthora infestans RXLR effector Pi17316 to promote disease. Plant Physiol. 177, 398–410 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. King, S. R. F. et al. Phytophthora infestans RXLR effector PexRD2 interacts with host MAPKKKε to suppress plant immune signaling. Plant Cell 26, 1345–1359 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Hu, T. et al. βC1 protein encoded in geminivirus satellite concertedly targets MKK2 and MPK4 to counter host defense. PLoS Pathog. 15, e1007728 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Doyle, E. L., Stoddard, B. L., Voytas, D. F. & Bogdanove, A. J. TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol. 23, 390–398 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Kim, S. et al. Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming. Nat. Commun. 11, 5845 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Song, T. et al. An Oomycete CRN effector reprograms expression of plant HSP genes by targeting their promoters. PLoS Pathog. 11, e1005348 (2015).

    PubMed  PubMed Central  Google Scholar 

  86. Canonne, J. et al. The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. Plant Cell 23, 3498–3511 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Chen, H. et al. A bacterial type III effector targets the master regulator of salicylic acid signaling, NPR1, to subvert plant immunity. Cell Host Microbe 22, 777–788 (2017).

    CAS  PubMed  Google Scholar 

  88. Li, Q. et al. A Phytophthora capsici virulence effector associates with NPR1 and suppresses plant immune responses. Phytopathol. Res. 1, 6 (2019).

    Google Scholar 

  89. Hou, Y. et al. SAPK10-mediated phosphorylation on WRKY72 releases its suppression on jasmonic acid biosynthesis and bacterial blight resistance. iScience 16, 499–510 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Li, H. et al. A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility. eLife 7, e40039 (2018).

    PubMed  PubMed Central  Google Scholar 

  91. Kong, L. et al. A Phytophthora effector manipulates hosthistone acetylation and reprograms defense gene expression to promote infection. Curr. Biol. 27, 981–991 (2017).

    CAS  PubMed  Google Scholar 

  92. Huang, J. et al. Phytophthora effectors modulate genome-wide alternative splicing of host mRNAs to reprogram plant immunity. Mol. Plant 13, 1470–1484 (2020).

    CAS  PubMed  Google Scholar 

  93. Caillaud, M.-C. et al. A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex. PLoS Biol. 14, e1001732 (2016).

    Google Scholar 

  94. Fu, Z. Q. et al. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284–288 (2007).

    CAS  PubMed  Google Scholar 

  95. Koda, Y. et al. Similarities of the biological activities of coronatine and coronafacic acid to those of jasmonic acid. Phytochemistry 41, 93–96 (1996).

    CAS  Google Scholar 

  96. Zheng, X.-Y. et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587–596 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Katsir, L., Schilmiller, A. L., Staswick, P. E., He, S. Y. & Howe, G. A. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl Acad. Sci. USA 105, 7100–7105 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Sakata, N., Ishiga, T., Masuo, S., Hashimoto, Y. & Ishiga, Y. Coronatine contributes to Pseudomonas cannabina pv. alisalensis virulence by overcoming both stomatal and apoplastic defenses in dicot and monocot plants. Mol. Plant Microbe Interact. 34, 746–757 (2021).

    PubMed  Google Scholar 

  99. Djamei, A. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398 (2011).

    CAS  PubMed  Google Scholar 

  100. Liu, T. et al. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5, 4686 (2014).

    CAS  PubMed  Google Scholar 

  101. Medina-Puche, L. et al. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182, 1109–1124 (2020).

    CAS  PubMed  Google Scholar 

  102. Yang, B. et al. The Phytophthora sojae RXLR effector Avh238 destabilizes soybean type2 GmACSs to suppress ethylene biosynthesis and promote infection. N. Phytol. 222, 425–437 (2018).

    Google Scholar 

  103. Patkar, R. N. et al. A fungal monooxygenase-derived jasmonate attenuates host innate immunity. Nat. Chem. Biol. 11, 733–740 (2015).

    CAS  PubMed  Google Scholar 

  104. Jia, Q. et al. CLCuMuB βC1 subverts ubiquitination by interacting with NbSKP1s to enhance geminivirus infection in Nicotiana benthamiana. PLoS Pathog. 12, e1005668 (2016).

    PubMed  PubMed Central  Google Scholar 

  105. Gimenez-Ibanez, S. et al. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS Biol. 12, e1001792 (2014).

    PubMed  PubMed Central  Google Scholar 

  106. Chen, Z. et al. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl Acad. Sci. USA 104, 20131–20136 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Bacete, L., Mélida, H., Miedes, E. & Molina, A. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J. 93, 614–636 (2018).

    CAS  PubMed  Google Scholar 

  108. Molina, A. et al. Arabidopsis cell wall composition determines disease resistance specificity and fitness. Proc. Natl Acad. Sci. USA 118, e2010243118 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Tanaka, S. et al. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3, e01355 (2014).

    PubMed  PubMed Central  Google Scholar 

  110. Seybold, H. et al. A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition. Nat. Commun. 11, 1910 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Kubicek, C. P., Starr, T. L. & Glass, N. L. Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi. Annu. Rev. Phytopathol. 52, 427–451 (2014).

    PubMed  Google Scholar 

  112. Sabbadin, F. et al. Secreted pectin monooxygenases drive plant infection by pathogenic oomycetes. Science 373, 774–779 (2021).

    CAS  PubMed  Google Scholar 

  113. Chen, L.-H. et al. A diverse member of the fungal Avr4 effector family interacts with de-esterified pectin in plant cell walls to disrupt their integrity. Sci. Adv. 7, eabe0809 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Ma, Z. et al. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355, 710–714 (2017).

    CAS  PubMed  Google Scholar 

  115. Bouwmeester, K. et al. The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog. 7, e1001327 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Kruger, J. et al. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296, 744–747 (2002).

    PubMed  Google Scholar 

  117. Paulus, J. K. et al. Extracellular proteolytic cascade in tomato activates immune protease Rcr3. Proc. Natl Acad. Sci. USA 117, 17409–17417 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Wang, S. et al. Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity. N. Phytol. 229, 3424–3439 (2021). This article describes the secretion of protease inhibitors by P. infestans to prevent the processing of the apoplastic effector PC2 by host subtilases and thereby block activation of PTI.

    CAS  Google Scholar 

  119. Ziemann, S. et al. An apoplastic peptide activates salicylic acid signalling in maize. Nat. Plants 4, 172–180 (2018).

    CAS  PubMed  Google Scholar 

  120. Bozkurt, T. O. et al. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl Acad. Sci. USA 108, 20832–20837 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Guo, B. et al. Phytophthora sojae effector PsAvh240 inhibits a host aspartic protease secretion to promote infection. Mol. Plant 12, 552–564 (2019).

    CAS  PubMed  Google Scholar 

  122. Wang, H. et al. An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection. PLoS Pathog. 17, e1010104 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Misas Villamil, J. C. et al. A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif. Nat. Commun. 10, 1576 (2019).

    PubMed  PubMed Central  Google Scholar 

  124. Chen, H., Raffaele, S. & Dong, S. Silent control: microbial plant pathogens evade host immunity without coding sequence changes. FEMS Microbiol. Rev. 45, fuab002 (2021).

    CAS  PubMed  Google Scholar 

  125. Xia, Y. et al. N-glycosylation shields Phytophthora sojae apoplastic effector PsXEG1 from a specific host aspartic protease. Proc. Natl Acad. Sci. USA 117, 27685–27693 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Ökmen, B. et al. Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato. N. Phytol. 198, 1203–1214 (2013).

    Google Scholar 

  127. Ma, L.-S. et al. The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins. Nat. Commun. 9, 1711 (2018). This article reports that U. maydis secretes the apoplastic effector Rsp3 to block the antifungal activity of the maize DUF26-domain family proteins.

    PubMed  PubMed Central  Google Scholar 

  128. Fones, H. & Preston, G. M. Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiol. Lett. 327, 1–8 (2012).

    CAS  PubMed  Google Scholar 

  129. Freitag, J., Ast, J. & Boelker, M. Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485, 522–U135 (2012).

    CAS  PubMed  Google Scholar 

  130. Nie, W. et al. A-to-I RNA editing in bacteria increases pathogenicity and tolerance to oxidative stress. PLoS Pathog. 16, e1008740 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M. & Doehlemann, G. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog. 8, e1002684 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Singh, R. et al. Magnaporthe oryzae effector AVR-Pii helps to establish compatibility by inhibition of the rice NADP-malic enzyme resulting in disruption of oxidative burst and host innate immunity. Mol. Cell 39, 426–438 (2016).

    CAS  Google Scholar 

  133. Dong, S. et al. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. PLoS Pathog. 7, e1002353 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Shidore, T. et al. The effector AvrRxo1 phosphorylates NAD in planta. PLoS Pathog. 13, e1006442 (2017).

    PubMed  PubMed Central  Google Scholar 

  135. Ai, G. et al. A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling. PLoS Pathog. 17, e1009388 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Zhang, Z., Catherine, H. & Gurr, S. J. Blumeria graminis secretes an extracellular catalase during infection of barley: potential role in suppression of host defence. Mol. Plant Pathol. 5, 537–547 (2004).

    CAS  PubMed  Google Scholar 

  137. Zhang, M. et al. Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol. 167, 164–175 (2014).

    PubMed  PubMed Central  Google Scholar 

  138. Csorba, T., Kontra, L. & Burgyán, J. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480, 85–103 (2015).

    PubMed  Google Scholar 

  139. Zhang, T. et al. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2, 16153 (2016).

    CAS  PubMed  Google Scholar 

  140. Cai, Q. et al. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360, 1126–1129 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Hou, Y. et al. A Phytophthora effector suppresses trans-kingdom RNAi to promote disease susceptibility. Cell Host Microbe 25, 153–165.e5 (2019).

    CAS  PubMed  Google Scholar 

  142. Qiao, Y. et al. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45, 330–333 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Landeo-Ríos, Y., Navas-Castillo, J., Moriones, E. & Cañizares, M. C. The p22 RNA silencing suppressor of the crinivirus Tomato chlorosis virus preferentially binds long dsRNAs preventing them from cleavage. Virology 488, 129–136 (2016).

    PubMed  Google Scholar 

  144. Chiu, M.-H., Chen, I.-H., Baulcombe, D. C. & Tsai, C.-H. The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 11, 641–649 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Lakatos, L. et al. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768–2780 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Wang, Y. et al. A calmodulin-binding transcription factor links calcium signaling to antiviral RNAi defense in plants. Cell Host Microbe 29, 1393–1406.e7 (2021).

    CAS  PubMed  Google Scholar 

  147. Rosas-Diaz, T. et al. A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi. Proc. Natl Acad. Sci. USA 115, 1388–1393 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Weiberg, A. et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118–123 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Berendsen, R. L. et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 12, 1496–1507 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Yuan, J. et al. Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6, 156 (2018).

    PubMed  PubMed Central  Google Scholar 

  151. Chen, T. et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580, 653–657 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Pfeilmeier, S. et al. The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves. Nat. Microbiol. 6, 852–864 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  153. Snelders, N. C. et al. Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nat. Plants 6, 1365–1374 (2020).

    CAS  PubMed  Google Scholar 

  154. Liu, Y., Zhu, A., Tan, H., Cao, L. & Zhang, R. Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana. Microbiome 7, 74 (2019).

    PubMed  PubMed Central  Google Scholar 

  155. Duran, P. et al. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973–983 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Vleeshouwers, V. G. A. A. et al.Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49, 507–531 (2011).

    CAS  PubMed  Google Scholar 

  157. Luo, M. et al. A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol. 39, 561–566 (2021).

    CAS  PubMed  Google Scholar 

  158. Huang, H. et al. Stepwise artificial evolution of an Sw-5b immune receptor extends its resistance spectrum against resistance-breaking isolates of Tomato spotted wilt virus. Plant Biotechnol. J. 19, 2164–2176 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Farnham, G. & Baulcombe, D. C. Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. Proc. Natl Acad. Sci. USA 103, 18828–18833 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  160. De la Concepcion, J. C. et al. Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nat. Plants 4, 576–585 (2018).

    PubMed  Google Scholar 

  161. De la Concepcion, J. C. et al. Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife 8, e47713 (2019).

    PubMed  PubMed Central  Google Scholar 

  162. Shao, F. et al. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233 (2003). This article reports that cleavage of Arabidopsis PBS1 by the P. syringae effector AvrPphB activates RPS5-mediated resistance.

    CAS  PubMed  Google Scholar 

  163. Kim, S. H., Qi, D., Ashfield, T., Helm, M. & Innes, R. W. Using decoys to expand the recognition specificity of a plant disease resistance protein. Science 351, 684–687 (2016).

    CAS  PubMed  Google Scholar 

  164. Oliva, R. et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 37, 1344–1350 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors apologize to colleagues whose studies were not cited owing to space limitations. They thank X. Tao, S. Dong, Z. Ma, Y. Xia, J. Huang, G. Sun and J. Wu for helpful suggestions, and D. Lv, M. Zeng and Y. Xu for help in designing the draft figures. Yan Wang and Yuanchao Wang are supported by China National Natural Science Foundation grants 31721004, 32020103012 and 31872927 and the grant for Distinguished Young Scholars of Jiangsu Province BK20190027. R.N.P. and T.N. are supported by Deutsche Forschungsgemeinschaft grant Nu70/16-1.

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Authors and Affiliations

  1. Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China

    Yan Wang & Yuanchao Wang

  2. The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China

    Yan Wang & Yuanchao Wang

  3. Centre for Molecular Biology of Plants (ZMBP), University of Tübingen, Tübingen, Germany

    Rory N. Pruitt & Thorsten Nürnberger

  4. Department of Biochemistry, University of Johannesburg, Johannesburg, South Africa

    Thorsten Nürnberger

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Yan Wang and R.N.P. researched data for the article. Yuanchao Wang, Yan Wang, R.N.P. and T.N. contributed to the discussion of content, wrote the article, and reviewed and edited the article.

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Glossary

Disease triangle

A paradigm describing the interactions among the three casual factors (the environment, the host and pathogens) governing plant disease. Plant disease occurs only when pathogenic microorganisms encounter susceptible plants under favourable environmental conditions.

Microbe-associated molecular patterns

(MAMPs). Structurally conserved microorganism-derived signature molecules, including peptides, carbohydrates or fatty acids, that are detected by surface-localized host cell receptors to activate plant defence.

Apoplast

The extracellular matrix outside plant plasma membranes, including cell walls and the intercellular space.

Helper NLRs

(hNLRs). NOD-like receptors (NLRs) that act as regulatory nodes controlling immune signalling downstream of sensor NLRs.

Sensor NLRs

NOD-like receptors (NLRs) that bind to or perceive effectors directly or indirectly by monitoring modifications in host targets.

Epistatic effectors

Microbial effectors that are genetically suppressive with regard to the activity or expression of other effectors.

Guardees

Plant proteins that are targeted by microbial effectors and are monitored by plant immune receptors.

Decoys

Mimic proteins in plants or microbial pathogens that are dispensable for microbial virulence in the absence of the cognate effectors or immune receptors.

Biotrophic pathogens

Pathogens that survive only in living plant cells without killing hosts during infection. Pathogens of this type often cannot be extensively cultured in vitro.

Necrotrophic pathogens

Pathogens that kill host cells and feed on dead or dying tissues throughout the life cycle.

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Wang, Y., Pruitt, R.N., Nürnberger, T. et al. Evasion of plant immunity by microbial pathogens. Nat Rev Microbiol 20, 449–464 (2022). https://doi.org/10.1038/s41579-022-00710-3

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