Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Regulation of pattern recognition receptor signalling in plants

Key Points

  • Plants rely on a cell-autonomous innate immune system to detect the presence of microorganisms and activate immune responses that deter infection. Recognition of conserved microbial features occurs essentially at the cell surface by means of transmembrane pattern recognition receptors (PRRs).

  • PRRs are part of multimeric protein complexes at the plasma membrane, differentially recruiting cytoplasmic kinases that connect PRR complexes to downstream signalling components.

  • Ligand binding initiates a series of phosphorylation events within PRR complexes that activates cellular immune signalling, which includes bursts of intracellular reactive oxygen species and calcium, activation of cytoplasmic kinase cascades, and transcriptional reprogramming.

  • As in mammals, excessive activation of plant immune responses can have detrimental consequences. Thus, a complex negative regulatory system controls different immune components to maintain cellular homeostasis.

  • Bacterial pathogens are able to subvert the plant immune system by secreting molecules, such as effectors, that often mimic the mode-of-action of host negative regulators of immune signalling.

Abstract

Recognition of pathogen-derived molecules by pattern recognition receptors (PRRs) is a common feature of both animal and plant innate immune systems. In plants, PRR signalling is initiated at the cell surface by kinase complexes, resulting in the activation of immune responses that ward off microorganisms. However, the activation and amplitude of innate immune responses must be tightly controlled. In this Review, we summarize our knowledge of the early signalling events that follow PRR activation and describe the mechanisms that fine-tune immune signalling to maintain immune homeostasis. We also illustrate the mechanisms used by pathogens to inhibit innate immune signalling and discuss how the innate ability of plant cells to monitor the integrity of key immune components can lead to autoimmune phenotypes following genetic or pathogen-induced perturbations of these components.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Recruitment of regulatory receptor kinases and RLCKs by PRRs in Arabidopsis and rice.
Figure 2: Early branching of PRR-triggered immunity signalling.
Figure 3: Negative regulation of PTI signalling by a multi-layered system.
Figure 4: Negative regulation at the PRR complex level.

References

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

    Article  CAS  Google Scholar 

  2. Dangl, J. L., Horvath, D. M. & Staskawicz, B. J. Pivoting the plant immune system from dissection to deployment. Science 341, 746–751 (2013).

    Article  CAS  PubMed  Google Scholar 

  3. Zipfel, C. Plant pattern-recognition receptors. Trends Immunol. 35, 345–351 (2014).

    Article  CAS  PubMed  Google Scholar 

  4. Bohm, H., Albert, I., Fan, L., Reinhard, A. & Nurnberger, T. Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol. 20, 47–54 (2014).

    Article  CAS  PubMed  Google Scholar 

  5. Gust, A. A. & Felix, G. Receptor like proteins associate with SOBIR1-type of adaptors to form bimolecular receptor kinases. Curr. Opin. Plant Biol. 21, 104–111 (2014).

    Article  CAS  PubMed  Google Scholar 

  6. Ranf, S. et al. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol. 16, 426–433 (2015).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Win, J. et al. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harbor Symp. Quant. Biol. 77, 235–247 (2012).

    Article  CAS  PubMed  Google Scholar 

  9. Dangl, J. L. & Jones, J. D. Plant pathogens and integrated defence responses to infection. Nature 411, 826–833 (2001).

    Article  CAS  PubMed  Google Scholar 

  10. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cesari, S., Bernoux, M., Moncuquet, P., Kroj, T. & Dodds, P. N. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front. Plant Sci. 5, 606 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wu, C. H., Krasileva, K. V., Banfield, M. J., Terauchi, R. & Kamoun, S. The “sensor domains” of plant NLR proteins: more than decoys? Front. Plant Sci. 6, 134 (2015).

    PubMed  PubMed Central  Google Scholar 

  13. Sarris, P. F., Cevik, V., Dagdas, G., Jones, J. D. & Krasileva, K. V. Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol. 14, 8 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kroj, T., Chanclud, E., Michel-Romiti, C., Grand, X. & Morel, J. B. Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol. 210, 618–626 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ding, S. W. RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632–644 (2010).

    Article  CAS  PubMed  Google Scholar 

  16. Korner, C. J. et al. The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol. Plant Microbe Interact. 26, 1271–1280 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Zorzatto, C. et al. NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 520, 679–682 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Niehl, A., Wyrsch, I., Boller, T. & Heinlein, M. Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol. http://dx.doi.org/10.1111/nph.13944 (2016).

  19. Guo, H., Callaway, J. B. & Ting, J. P. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21, 677–687 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ronald, P. C. & Beutler, B. Plant and animal sensors of conserved microbial signatures. Science 330, 1061–1064 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. Ausubel, F. M. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6, 973–979 (2005).

    Article  CAS  PubMed  Google Scholar 

  22. Maekawa, T., Kufer, T. A. & Schulze-Lefert, P. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817–826 (2011).

    Article  CAS  PubMed  Google Scholar 

  23. Zipfel, C. & Felix, G. Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8, 353–360 (2005).

    Article  CAS  PubMed  Google Scholar 

  24. Neyen, C. & Lemaitre, B. Sensing Gram-negative bacteria: a phylogenetic perspective. Curr. Opin. Immunol. 38, 8–17 (2016).

    Article  CAS  PubMed  Google Scholar 

  25. Cao, X. Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nat. Rev. Immunol. 16, 35–50 (2015).

    Article  CAS  Google Scholar 

  26. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373–384 (2010).

    Article  CAS  PubMed  Google Scholar 

  27. O'Neill, L. A. & Bowie, A. G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7, 353–364 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Macho, A. P. & Zipfel, C. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54, 263–272 (2014).

    Article  CAS  PubMed  Google Scholar 

  29. Shiu, S. H. & Bleecker, A. B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl Acad. Sci. USA 98, 10763–10768 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Thaiss, C. A., Levy, M., Itav, S. & Elinav, E. Integration of innate immune signaling. Trend Immunol. 37, 84–101 (2016).

    Article  CAS  Google Scholar 

  31. Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007). References 31 and 32 revealed the importance of BAK1 in plant innate immunity by demonstrating that it forms a complex with FLS2 following ligand perception to initiate immune signalling.

    Article  CAS  PubMed  Google Scholar 

  33. Schulze, B. et al. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444–9451 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Roux, M. et al. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440–2455 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Sun, Y. et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624–628 (2013). This was the first report of a crystal structure of a ligand-bound plant PRR, which revealed that BAK1 acts as a co-receptor by participating in flagellin binding together with the main receptor FLS2.

    Article  CAS  PubMed  Google Scholar 

  36. Tang, J. et al. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res. 25, 110–120 (2015).

    Article  CAS  PubMed  Google Scholar 

  37. Somssich, M. et al. Real-time dynamics of peptide ligand-dependent receptor complex formation in planta. Sci. Signal. 8, ra76 (2015).

    Article  CAS  PubMed  Google Scholar 

  38. Sun, W. et al. Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24, 1096–1113 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Liebrand, T. W., van den Burg, H. A. & Joosten, M. H. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 19, 123–132 (2014).

    Article  CAS  PubMed  Google Scholar 

  40. Schwessinger, B. & Rathjen, J. P. Changing SERKs and priorities during plant life. Trends Plant Sci. 20, 531–533 (2015).

    Article  CAS  PubMed  Google Scholar 

  41. Santiago, J., Henzler, C. & Hothorn, M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341, 889–892 (2013).

    Article  CAS  PubMed  Google Scholar 

  42. Sun, Y. et al. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res. 23, 1326–1329 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang, J. et al. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525, 265–268 (2015).

    Article  CAS  PubMed  Google Scholar 

  44. Meng, X. et al. Differential function of arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr. Biol. 25, 2361–2372 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Meng, X. et al. Ligand-induced receptor-like kinase complex regulates floral organ abscission in arabidopsis. Cell Rep. 14, 1330–1338 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Santiago, J. et al. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5, e15075 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Albert, I. et al. An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1, 15140 (2015).

    Article  CAS  PubMed  Google Scholar 

  48. Postma, J. et al. Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol. 210, 627–642 (2016).

    Article  CAS  PubMed  Google Scholar 

  49. Liebrand, T. W. et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl Acad. Sci. USA 110, 10010–10015 (2013).

    Article  PubMed  Google Scholar 

  50. Zhang, W. et al. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25, 4227–4241 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Jehle, A. K., Furst, U., Lipschis, M., Albert, M. & Felix, G. Perception of the novel MAMP eMax from different Xanthomonas species requires the Arabidopsis receptor-like protein ReMAX and the receptor kinase SOBIR. Plant Sign. Behav. 8, e27408 (2013).

    Article  CAS  Google Scholar 

  52. Bi, G. et al. Arabidopsis thaliana receptor-like protein AtRLP23 associates with the receptor-like kinase AtSOBIR1. Plant Sign. Behav. 9, e27937 (2014).

    Article  CAS  Google Scholar 

  53. Peng, K. C., Wang, C. W., Wu, C. H., Huang, C. T. & Liou, R. F. Tomato SOBIR1/EVR homologs are involved in elicitin perception and plant defense against the oomycete pathogen phytophthora parasitica. Mol. Plant Microbe Interact. 28, 913–926 (2015).

    Article  CAS  PubMed  Google Scholar 

  54. Ma, L. & Borhan, M. H. The receptor-like kinase SOBIR1 interacts with Brassica napus LepR3 and is required for Leptosphaeria maculans AvrLm1-triggered immunity. Front. Plant Sci. 6, 933 (2015).

    PubMed  PubMed Central  Google Scholar 

  55. Zhang, L. et al. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Phys. 164, 352–364 (2014).

    Article  CAS  Google Scholar 

  56. Chen, X. et al. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol. Plant 7, 874–892 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Pruitt, R. N. et al. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. 1, e1500245 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. He, K. et al. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 1109–1115 (2007).

    Article  CAS  PubMed  Google Scholar 

  59. de Oliveira, M. V. V. et al. Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat. Plants 2, 15218 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Rodriguez, E., El Ghoul, H., Mundy, J. & Petersen, M. Making sense of plant autoimmunity and 'negative regulators'. FEBS J. 283, 1385–1391 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Shimizu, T. et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204–214 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hayafune, M. et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl Acad. Sci. USA 111, E404–E413 (2014).

    Article  CAS  PubMed  Google Scholar 

  63. Liu, B. et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24, 3406–3419 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Ao, Y. et al. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J. 80, 1072–1084 (2014).

    Article  CAS  PubMed  Google Scholar 

  65. Liu, T. et al. Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160–1164 (2012).

    Article  CAS  PubMed  Google Scholar 

  66. Petutschnig, E. K., Jones, A. M., Serazetdinova, L., Lipka, U. & Lipka, V. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285, 28902–28911 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Miya, A. et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 104, 19613–19618 (2007).

    Article  PubMed  Google Scholar 

  68. 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 http://dx.doi.org/10.7554/eLife.03766 (2014). This paper identified LYK5 as a high-affinity chitin-binding receptor in Arabidopsis and proposed CERK1 to act as the co-receptor.

  69. Wan, J. et al. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Phys. 160, 396–406 (2012).

    Article  CAS  Google Scholar 

  70. Willmann, R. et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl Acad. Sci. USA 108, 19824–19829 (2011).

    Article  PubMed  Google Scholar 

  71. Gimenez-Ibanez, S., Ntoukakis, V. & Rathjen, J. P. The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Sign. Behav. 4, 539–541 (2009).

    Article  CAS  Google Scholar 

  72. Gimenez-Ibanez, S. et al. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423–429 (2009).

    Article  CAS  PubMed  Google Scholar 

  73. Faulkner, C. et al. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl Acad. Sci. USA 110, 9166–9170 (2013).

    Article  PubMed  Google Scholar 

  74. Wan, J. et al. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20, 471–481 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lehti-Shiu, M. D., Zou, C., Hanada, K. & Shiu, S. H. Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Phys. 150, 12–26 (2009).

    Article  CAS  Google Scholar 

  76. 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).

    Article  CAS  PubMed  Google Scholar 

  77. Lu, D. et al. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl Acad. Sci. USA 107, 496–501 (2010). Referencces 76 and 77 provided the first evidence that cytoplasmic kinases, in particular BIK1, act as key immune signal transducers immediately downstream of PRRs.

    Article  PubMed  Google Scholar 

  78. Liu, Z. et al. BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc. Natl Acad. Sci. USA 110, 6205–6210 (2013).

    Article  CAS  PubMed  Google Scholar 

  79. Sreekanta, S. et al. The receptor-like cytoplasmic kinase PCRK1 contributes to pattern-triggered immunity against Pseudomonas syringae in Arabidopsis thaliana. New Phytol. 207, 78–90 (2015).

    Article  CAS  PubMed  Google Scholar 

  80. Yamaguchi, K. et al. A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13, 347–357 (2013).

    Article  CAS  PubMed  Google Scholar 

  81. Shinya, T. et al. Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J. 79, 56–66 (2014).

    Article  CAS  PubMed  Google Scholar 

  82. Shi, H. et al. BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25, 1143–1157 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Boller, T. & Felix, G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406 (2009).

    Article  CAS  PubMed  Google Scholar 

  84. Seybold, H. et al. Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol. 204, 782–790 (2014).

    Article  CAS  PubMed  Google Scholar 

  85. Lee, J., Eschen-Lippold, L., Lassowskat, I., Bottcher, C. & Scheel, D. Cellular reprogramming through mitogen-activated protein kinases. Front. Plant Sci. 6, 940 (2015).

    PubMed  PubMed Central  Google Scholar 

  86. Kadota, Y. et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54, 43–55 (2014).

    Article  CAS  PubMed  Google Scholar 

  87. Li, L. et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329–338 (2014). References 86 and 87 identified for the first time a downstream substrate of the cytoplasmic kinase BIK1, revealing a direct link between activated PRR complexes and activation of a cellular immune output.

    Article  CAS  PubMed  Google Scholar 

  88. Lin, Z. D., Liebrand, T. W., Yadeta, K. A. & Coaker, G. L. PBL13 is a serine/threonine protein kinase that negatively regulates Arabidopsis immune responses. Plant Phys. 169, 2950–2962 (2015).

    CAS  Google Scholar 

  89. Ogasawara, Y. et al. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J. Biol. Chem. 283, 8885–8892 (2008).

    Article  CAS  PubMed  Google Scholar 

  90. Oda, T. et al. Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. J. Biol. Chem. 285, 1435–1445 (2010).

    Article  CAS  PubMed  Google Scholar 

  91. Kobayashi, M. et al. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065–1080 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Dubiella, U. et al. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl Acad. Sci. USA 110, 8744–8749 (2013).

    Article  PubMed  Google Scholar 

  93. Boudsocq, M. et al. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464, 418–422 (2010). This study revealed a group of closely-related calcium-dependent protein kinases as being crucial for the activation of specific sets of immune responses.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kadota, Y., Shirasu, K. & Zipfel, C. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol. 56, 1472–1480 (2015).

    Article  CAS  PubMed  Google Scholar 

  95. Liang, X. et al. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. eLife 5, e13568 (2016). This study revealed the role of an FLS2-associated heterotrimeric G protein complex in the regulation of immune signalling by controlling BIK1 protein levels.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Wong, H. L. et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022–4034 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Akamatsu, A. et al. An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13, 465–476 (2013). This study identified a small G protein module as the first direct downstream substrate of a PRR complex in plants.

    Article  CAS  PubMed  Google Scholar 

  98. Ranf, S. et al. Microbe-associated molecular pattern-induced calcium signaling requires the receptor-like cytoplasmic kinases, PBL1 and BIK1. BMC Plant Biol. 14, 374 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Monaghan, J., Matschi, S., Romeis, T. & Zipfel, C. The calcium-dependent protein kinase CPK28 negatively regulates the BIK1-mediated PAMP-induced calcium burst. Plant Sign. Behav. 10, e1018497 (2015).

    Article  CAS  Google Scholar 

  100. Gravino, M., Savatin, D. V., Macone, A. & De Lorenzo, G. Ethylene production in Botrytis cinerea- and oligogalacturonide-induced immunity requires calcium-dependent protein kinases. Plant J. 84, 1073–1086 (2015).

    Article  CAS  PubMed  Google Scholar 

  101. Gao, X. et al. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog. 9, e1003127 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983 (2002).

    Article  CAS  PubMed  Google Scholar 

  103. Suarez-Rodriguez, M. C. et al. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Phys. 143, 661–669 (2007).

    Article  CAS  Google Scholar 

  104. Gao, M. et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190–1198 (2008).

    Article  CAS  PubMed  Google Scholar 

  105. Bethke, G. et al. Activation of the Arabidopsis thaliana mitogen-activated protein kinase MPK11 by the flagellin-derived elicitor peptide, flg22. Mol. Plant Microbe Interact. 25, 471–480 (2012).

    Article  CAS  PubMed  Google Scholar 

  106. Meszaros, T. et al. The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J. 48, 485–498 (2006).

    Article  CAS  PubMed  Google Scholar 

  107. Petersen, M. et al. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120 (2000).

    Article  CAS  PubMed  Google Scholar 

  108. Kong, Q. et al. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24, 2225–2236 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Roux, M. E. et al. The mRNA decay factor PAT1 functions in a pathway including MAP kinase 4 and immune receptor SUMM2. EMBO J. 34, 593–608 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Zhang, Z. et al. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253–263 (2012). This study demonstrated that the integrity of the MPK4 cascade is guarded by an NLR, which enabled documenting the positive role of MPK4 in plant immune signalling.

    Article  CAS  PubMed  Google Scholar 

  111. Frei dit Frey, N. et al. Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences. Genome Biol. 15, R87 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Berriri, S. et al. Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. Plant Cell 24, 4281–4293 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Feng, F. et al. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485, 114–118 (2012). This paper described how a bacterial effector disrupts the kinase activity of the central immune regulator BIK1 in order to supress host immune signalling.

    Article  CAS  PubMed  Google Scholar 

  114. Cheng, Z. Y. et al. Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521, 213–216 (2015). This study showed that activation of immune responses by bacterial secreted proteases involves an heterotrimeric G protein complex.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Meng, X. & Zhang, S. MAPK cascades in plant disease resistance signaling. Ann. Rev. Phytopathol. 51, 245–266 (2013).

    Article  CAS  Google Scholar 

  116. Goldszmid, R. S. & Trinchieri, G. The price of immunity. Nat. Immunol. 13, 932–938 (2012).

    Article  CAS  PubMed  Google Scholar 

  117. Murray, P. J. & Smale, S. T. Restraint of inflammatory signaling by interdependent strata of negative regulatory pathways. Nat. Immunol. 13, 916–924 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Castells, E. & Casacuberta, J. M. Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. J. Exp. Bot. 58, 3503–3511 (2007).

    Article  CAS  PubMed  Google Scholar 

  119. Zeqiraj, E. & van Aalten, D. M. F. Pseudokinases-remnants of evolution or key allosteric regulators? Curr. Opin. Struc. Biol. 20, 772–781 (2010).

    Article  CAS  Google Scholar 

  120. Mendrola, J. M., Shi, F., Park, J. H. & Lemmon, M. A. Receptor tyrosine kinases with intracellular pseudokinase domains. Biochem. Soc. Trans. 41, 1029–1036 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Boudeau, J., Miranda-Saavedra, D., Barton, G. J. & Alessi, D. R. Emerging roles of pseudokinases. Trends Cell Biol. 16, 443–452 (2006).

    Article  CAS  PubMed  Google Scholar 

  122. Shaw, A. S., Kornev, A. P., Hu, J., Ahuja, L. G. & Taylor, S. S. Kinases and pseudokinases: lessons from RAF. Mol. Cell. Biol. 34, 1538–1546 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kobayashi, K. et al. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191–202 (2002).

    Article  CAS  PubMed  Google Scholar 

  124. Hubbard, L. L. & Moore, B. B. IRAK-M regulation and function in host defense and immune homeostasis. Infect. Dis. Rep. 2, e9 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Gao, M. et al. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6, 34–44 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. Halter, T. et al. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24, 134–143 (2014). This study demonstrated a novel mechanism by which the pseudokinase BIR2 negatively regulates immune signalling by preventing the association of FLS2 and BAK1.

    Article  CAS  PubMed  Google Scholar 

  127. Blaum, B. S. et al. Structure of the pseudokinase domain of BIR2, a regulator of BAK1-mediated immune signaling in Arabidopsis. J. Struct. Biol. 186, 112–121 (2014).

    Article  CAS  PubMed  Google Scholar 

  128. Li, S. Y., Strelow, A., Fontana, E. J. & Wesche, H. IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl Acad. Sci. USA 99, 5567–5572 (2002).

    Article  CAS  PubMed  Google Scholar 

  129. Ferrao, R. et al. IRAK4 dimerization and trans-autophosphorylation are induced by myddosome assembly. Mol. Cell 55, 891–903 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Lin, W. et al. Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc. Natl Acad. Sci. USA 111, 3632–3637 (2014).

    Article  CAS  PubMed  Google Scholar 

  131. Schwessinger, B. et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Gen. 7, e1002046 (2011).

    Article  CAS  Google Scholar 

  132. Felix, G., Regenass, M., Spanu, P. & Boller, T. The protein phosphatase inhibitor calyculin A mimics elicitor action in plant cells and induces rapid hyperphosphorylation of specific proteins as revealed by pulse labeling with [33P]phosphate. Proc. Natl Acad. Sci. USA 91, 952–956 (1994).

    Article  CAS  PubMed  Google Scholar 

  133. Chandra, S. & Low, P. S. Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proc. Natl Acad. Sci. USA 92, 4120–4123 (1995).

    Article  CAS  PubMed  Google Scholar 

  134. Park, C. J. et al. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol. 6, e231 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Chen, X. et al. An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21-mediated immunity. Proc. Natl Acad. Sci. USA 107, 8029–8034 (2010).

    Article  PubMed  Google Scholar 

  136. Gomez-Gomez, L., Bauer, Z. & Boller, T. Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13, 1155–1163 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Ding, Z. et al. Phosphoprotein and phosphopeptide interactions with the FHA domain from Arabidopsis kinase-associated protein phosphatase. Biochemistry 46, 2684–2696 (2007).

    Article  CAS  PubMed  Google Scholar 

  138. Segonzac, C. et al. Negative control of BAK1 by protein phosphatase 2A during plant innate immunity. EMBO J. 33, 2069–2079 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Mithoe, S. C. et al. Attenuation of pattern recognition receptor signaling is mediated by a MAP kinase kinase kinase. EMBO rep. 17, 441–454 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Heride, C., Urbe, S. & Clague, M. J. Ubiquitin code assembly and disassembly. Curr. Biol. 24, R215–R220 (2014).

    Article  CAS  PubMed  Google Scholar 

  141. Kondo, T., Kawai, T. & Akira, S. Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol. 33, 449–458 (2012).

    Article  CAS  PubMed  Google Scholar 

  142. Trujillo, M., Ichimura, K., Casais, C. & Shirasu, K. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr. Biol. 18, 1396–1401 (2008).

    Article  CAS  PubMed  Google Scholar 

  143. Stegmann, M. et al. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24, 4703–4716 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Lu, D. et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332, 1439–1442 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Ben Khaled, S., Postma, J. & Robatzek, S. A moving view: subcellular trafficking processes in pattern recognition receptor-triggered plant immunity. Annu. Rev. Phytophatol. 53, 379–402 (2015).

    Article  CAS  Google Scholar 

  146. Smith, J. M. et al. Loss of Arabidopsis thaliana Dynamin-Related Protein 2B reveals separation of innate immune signaling pathways. PLoS Pathog. 10, e1004578 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Monaghan, J. et al. The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16, 605–615 (2014). This paper revealed the role of CPK28 in the regulation of proteasomal-dependent BIK1 turnover and demonstrates that BIK1 is a rate-limiting step for the activation of PRR-mediated immune signalling.

    Article  CAS  PubMed  Google Scholar 

  148. Tsuda, K. & Somssich, I. E. Transcriptional networks in plant immunity. New Phytol. 206, 932–947 (2015).

    Article  CAS  PubMed  Google Scholar 

  149. Arthur, J. S. & Ley, S. C. Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol. 13, 679–692 (2013).

    Article  CAS  PubMed  Google Scholar 

  150. Caunt, C. J. & Keyse, S. M. Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J. 280, 489–504 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Brock, A. K. et al. The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Phys. 153, 1098–1111 (2010).

    Article  CAS  Google Scholar 

  152. Galletti, R., Ferrari, S. & De Lorenzo, G. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Phys. 157, 804–814 (2011).

    Article  CAS  Google Scholar 

  153. Schweighofer, A. et al. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 19, 2213–2224 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Anderson, J. C. et al. Arabidopsis MAP Kinase Phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant J. 67, 258–268 (2011).

    Article  CAS  PubMed  Google Scholar 

  155. Bartels, S. et al. MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21, 2884–2897 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Lumbreras, V. et al. MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J. 63, 1017–1030 (2010).

    Article  CAS  PubMed  Google Scholar 

  157. Qiu, J. L. et al. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27, 2214–2221 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mao, G. et al. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639–1653 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Rasmussen, M. W., Roux, M., Petersen, M. & Mundy, J. MAP kinase cascades in Arabidopsis innate immunity. Front. Plant Sci. 3, 169 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  160. Weyhe, M., Eschen-Lippold, L., Pecher, P., Scheel, D. & Lee, J. Menage a trois: the complex relationships between mitogen-activated protein kinases, WRKY transcription factors, and VQ-motif-containing proteins. Plant Sign. Behav. 9, e29519 (2014).

    Article  CAS  Google Scholar 

  161. Cheng, Y. et al. Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Phys. 159, 810–825 (2012).

    Article  CAS  Google Scholar 

  162. Pecher, P. et al. The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of 'VQ-motif'-containing proteins to regulate immune responses. New Phytol. 203, 592–606 (2014).

    Article  CAS  PubMed  Google Scholar 

  163. Lai, Z. et al. Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23, 3824–3841 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Li, B. et al. Phosphorylation of trihelix transcriptional repressor ASR3 by MAP KINASE4 negatively regulates Arabidopsis immunity. Plant Cell 27, 839–856 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Buratowski, S. Progression through the RNA polymerase II CTD Cycle. Mol. Cell 36, 541–546 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Li, F. et al. Modulation of RNA polymerase II phosphorylation downstream of pathogen perception orchestrates plant immunity. Cell Host Microbe 16, 748–758 (2014). This study revealed that dynamic phosphorylation of the C-terminal domain of RNA polymerase II orchestrates immune gene expression in plants.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Gibson, B. A. & Kraus, W. L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell. Biol. 13, 411–424 (2012).

    Article  CAS  PubMed  Google Scholar 

  168. Song, J., Keppler, B. D., Wise, R. R. & Bent, A. F. PARP2 is the predominant poly(ADP-ribose) polymerase in Arabidopsis DNA damage and immune responses. PLoS Gen. 11, e1005200 (2015).

    Article  CAS  Google Scholar 

  169. Feng, B. et al. Protein poly(ADP-ribosyl)ation regulates Arabidopsis immune gene expression and defense responses. PLoS Gen. 11, e1004936 (2015).

    Article  CAS  Google Scholar 

  170. Pieterse, C. M., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S. C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489–521 (2012).

    Article  CAS  PubMed  Google Scholar 

  171. Yi, S. Y., Shirasu, K., Moon, J. S., Lee, S. G. & Kwon, S. Y. The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PloS One 9, e88951 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Tateda, C. et al. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26, 4171–4187 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Geng, X., Jin, L., Shimada, M., Kim, M. G. & Mackey, D. The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta 240, 1149–1165 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Boutrot, F. et al. Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc. Natl Acad. Sci. USA 107, 14502–14507 (2010).

    Article  PubMed  Google Scholar 

  175. Mishina, T. E. & Zeier, J. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500–513 (2007).

    Article  CAS  PubMed  Google Scholar 

  176. Felix, G., Duran, J. D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276 (1999).

    Article  CAS  PubMed  Google Scholar 

  177. Flury, P., Klauser, D., Schulze, B., Boller, T. & Bartels, S. The anticipation of danger: microbe-associated molecular pattern perception enhances AtPep-triggered oxidative burst. Plant Phys. 161, 2023–2035 (2013).

    Article  CAS  Google Scholar 

  178. Tintor, N. et al. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl Acad. Sci. USA 110, 6211–6216 (2013).

    Article  CAS  PubMed  Google Scholar 

  179. Robert-Seilaniantz, A., Grant, M. & Jones, J. D. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49, 317–343 (2011).

    Article  CAS  PubMed  Google Scholar 

  180. Navarro, L. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439 (2006).

    Article  CAS  PubMed  Google Scholar 

  181. Robert-Seilaniantz, A. et al. The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J. 67, 218–231 (2011).

    Article  CAS  PubMed  Google Scholar 

  182. Naseem, M., Wolfling, M. & Dandekar, T. Cytokinins for immunity beyond growth, galls and green islands. Trends Plant Sci. 19, 481–484 (2014).

    Article  CAS  PubMed  Google Scholar 

  183. Gohlke, J. & Deeken, R. Plant responses to Agrobacterium tumefaciens and crown gall development. Front. Plant Sci. 5, 155 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  184. Hann, D. R. et al. The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol. 201, 585–598 (2014).

    Article  CAS  PubMed  Google Scholar 

  185. Choi, J. et al. The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell 19, 284–295 (2010).

    Article  CAS  PubMed  Google Scholar 

  186. Albrecht, C. et al. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc. Natl Acad. Sci. USA 109, 303–308 (2012).

    Article  PubMed  Google Scholar 

  187. Belkhadir, Y. et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc. Natl Acad. Sci. USA 109, 297–302 (2012).

    Article  PubMed  Google Scholar 

  188. Lozano-Duran, R. et al. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2, e00983 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  189. Fan, M. et al. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26, 828–841 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Malinovsky, F. G. et al. Antagonistic regulation of growth and immunity by the Arabidopsis basic helix–loop–helix transcription factor homolog of brassinosteroid enhanced expression2 interacting with increased leaf inclination1 binding bHLH1. Plant Phys. 164, 1443–1455 (2014).

    Article  CAS  Google Scholar 

  191. Lozano-Duran, R. & Zipfel, C. Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci. 20, 12–19 (2015).

    Article  CAS  PubMed  Google Scholar 

  192. Jiménez-Góngora, T., Kim, S.-K., Lozano-Durán, R. & Zipfel, C. Flg22-triggered immunity negatively regulates key BR biosynthetic genes. Front. Plant Sci. 6, 981 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  193. Igarashi, D., Tsuda, K. & Katagiri, F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J. 71, 194–204 (2012).

    Article  CAS  PubMed  Google Scholar 

  194. Mosher, S. et al. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J. 73, 469–482 (2013).

    Article  CAS  PubMed  Google Scholar 

  195. Murray, P. J. The primary mechanism of the IL-10-regulated anti inflammatory response is to selectively inhibit transcription. Proc. Natl Acad. Sci. USA 102, 8686–8691 (2005).

    Article  CAS  PubMed  Google Scholar 

  196. Macho, A. P. & Zipfel, C. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23, 14–22 (2015).

    Article  CAS  PubMed  Google Scholar 

  197. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Xiang, T. et al. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18, 74–80 (2008).

    Article  CAS  PubMed  Google Scholar 

  199. Macho, A. P. et al. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343, 1509–1512 (2014). This study revealed the importance of tyrosine phosphorylation for the activation of the immune receptor EFR and how pathogenic bacteria inhibit this post-translational modification as a virulence strategy.

    Article  CAS  PubMed  Google Scholar 

  200. Wang, G. et al. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18, 285–295 (2015).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Shao, F. et al. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233 (2003).

    Article  CAS  PubMed  Google Scholar 

  204. 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).

    Article  CAS  PubMed  Google Scholar 

  205. Abramovitch, R. B., Janjusevic, R., Stebbins, C. E. & Martin, G. B. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc. Natl Acad. Sci. USA 103, 2851–2856 (2006).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  207. Zeng, L., Velasquez, A. C., Munkvold, K. R., Zhang, J. & Martin, G. B. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 69, 92–103 (2012).

    Article  CAS  PubMed  Google Scholar 

  208. Cheng, W. et al. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III Effector. Cell Host Microbe 10, 616–626 (2011).

    Article  CAS  PubMed  Google Scholar 

  209. Zhou, Z. et al. An arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion. Plant Cell 27, 2032–2041 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Lee, D., Bourdais, G., Yu, G., Robatzek, S. & Coaker, G. Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H+-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27, 2042–2056 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. 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).

    Article  CAS  PubMed  Google Scholar 

  212. Mackey, D., Holt, B. F., 3rd, Wiig, A. & Dangl, J. L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002).

    Article  CAS  PubMed  Google Scholar 

  213. Belkhadir, Y., Nimchuk, Z., Hubert, D. A., Mackey, D. & Dangl, J. L. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16, 2822–2835 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Jiang, S. et al. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 9, e1003715 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Holton, N., Nekrasov, V., Ronald, P. C., Zipfel, C. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathog. 11, e1004602 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Couto, D. et al. The Arabidopsis protein phosphatase PP2C38 negatively regulates the central immune kinase BIK1. PLoS Pathog. http://dx.doi.org/10.1371/journal.ppat.1005811 (2016).

Download references

Acknowledgements

The authors would like to thank all members of the Zipfel laboratory for fruitful discussions, especially N. Holton and M. Stegmann, as well as S. Ben Khaled, for critically reading the manuscript before submission. D.C. was supported by a Ph.D. scholarship (reference SFRH/BD/79088/2011) from Fundação para a Ciência e a Tecnologia (FCT). Research in the Zipfel laboratory is funded by the Gatsby Charitable Foundation, the European Research Council (ERC), the UK Biotechnology and Biological Sciences Research Council (BBSRC), and the Two Blades Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cyril Zipfel.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Receptor kinases

Plasma membrane-localized proteins characterized by a ligand-binding ectodomain, a single-pass transmembrane domain and an intracellular signalling kinase domain. Different types of ectodomain determine their ligand-binding specificity. Receptor kinases may act as the main receptor or as co-receptor or regulatory protein.

Receptor-like proteins

(RLPs). Surface-localized proteins similar to receptor kinases but lacking an obvious intracellular signalling domain. RLPs typically require regulatory receptor kinases to initiate signalling.

Plasmodesmata

Intercellular cytoplasmic bridges equivalent to gap junctions that allow communication and transport of molecules between plant cells. During pathogen infection, plasmodesmata can be sealed by deposition of callose layers to isolate infected areas.

Stomata

Natural openings in the leaf epidermis formed by two guard cells that enable gaseous exchange and are often used by pathogenic microorganisms to enter the leaf.

EF-hand motifs

Helix–loop–helix protein motifs involved in Ca2+ binding.

Callose

A (1,3)-β-glucan polymer present in the plant cell wall. Deposition of callose occurs upon pathogen recognition, forming cell wall thickenings.

Exocyst complex

An octameric complex involved in the tethering of exocytic vesicles to their site of fusion in the plasma membrane.

Phytoalexin

Antimicrobial compounds produced by plants during pathogen infection.

Camalexin

Typical Arabidopsis phytoalexin produced in response to pathogen infection; it is also known as 3-thiazol-2′-yl-indole.

VQ proteins

(VPQs). A class of plant-specific proteins with a conserved FxxφVQxφTG amino acid motif (VQ motif; x representing any amino acid and φ representing hydrophobic residues).

Salicylic acid

A phenolic plant hormone with a major role in plant defence against biotrophic pathogens. Its acetylated form (acetylsalicylic acid) is commonly known as aspirin, a widely prescribed anti-inflammatory drug.

Jasmonic acid

The best-studied member of the jasmonates family of oxylipin plant hormones. Jasmonates are typically synthesized during responses against necrotrophic pathogens and herbivores.

Auxin

A class of plant growth hormone, existing mostly as free or conjugated forms of indole-acetic acid (IAA), which is a tryptophan derivative. Auxin has a pivotal role in various key developmental processes, such as cell expansion and division, root and stem elongation, and flowering.

Cytokinins

Plant growth hormones, derived from adenine, that are known to promote cell division and differentiation.

Brassinosteroids

A class of polyhydroxysteroid plant hormone required for several developmental and physiological processes. Brassinosteroids are perceived at the cell surface by the leucine-rich repeat (LRR)- receptor kinase BRI1, which recruits the co-receptor BAK1 to initiate brassinosteroid-mediated signalling.

Gibberellin

Diterpene-type plant growth hormones involved in several developmental processes, such as seed germination, stem elongation and fruit maturation.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Couto, D., Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16, 537–552 (2016). https://doi.org/10.1038/nri.2016.77

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nri.2016.77

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing