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An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity

Nature Plants volume 1, Article number: 15140 (2015) Cite this article

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Abstract

Plants and animals employ innate immune systems to cope with microbial infection. Pattern-triggered immunity relies on the recognition of microbe-derived patterns by pattern recognition receptors (PRRs). Necrosis and ethylene-inducing peptide 1-like proteins (NLPs) constitute plant immunogenic patterns that are unique, as these proteins are produced by multiple prokaryotic (bacterial) and eukaryotic (fungal, oomycete) species. Here we show that the leucine-rich repeat receptor protein (LRR-RP) RLP23 binds in vivo to a conserved 20-amino-acid fragment found in most NLPs (nlp20), thereby mediating immune activation in Arabidopsis thaliana. RLP23 forms a constitutive, ligand-independent complex with the LRR receptor kinase (LRR-RK) SOBIR1 (Suppressor of Brassinosteroid insensitive 1 (BRI1)-associated kinase (BAK1)-interacting receptor kinase 1), and recruits a second LRR-RK, BAK1, into a tripartite complex upon ligand binding. Stable, ectopic expression of RLP23 in potato (Solanum tuberosum) confers nlp20 pattern recognition and enhanced immunity to destructive oomycete and fungal plant pathogens, such as Phytophthora infestans and Sclerotinia sclerotiorum. PRRs that recognize widespread microbial patterns might be particularly suited for engineering immunity in crop plants.

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Figure 1: RLP23 confers sensitivity to nlp20.
Figure 2: nlp20 interacts specifically with RLP23 in vitro a,b and in planta c,d.
Figure 3: RLP23 interacts with SOBIR1, BAK1 and other members of the SERK protein family, and these proteins are required for nlp20-mediated defence activation.
Figure 4: RLP23 physically interacts with SOBIR1 and BAK1.
Figure 5: RLP23-mediated pathogen resistance.

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References

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  3. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  Google Scholar 

  4. Nürnberger, T., Brunner, F., Kemmerling, B. & Piater, L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249–266 (2004).

    Article  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  Google Scholar 

  6. Dou, D. & Zhou, J. M. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484–495 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Thomma, B. P., Nürnberger, T. & Joosten, M. H. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4–15 (2011).

    Article  CAS  Google Scholar 

  9. 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).

    Article  CAS  Google Scholar 

  10. Zipfel, C. et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760 (2006).

    Article  CAS  Google Scholar 

  11. Joosten, M. H., Cozijnsen, T. J. & De Wit, P. J. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367, 384–386 (1994).

    Article  CAS  Google Scholar 

  12. Thomas, C. M. et al. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9, 2209–2224 (1997).

    Article  CAS  Google Scholar 

  13. Ron, M. & Avni, A. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16, 1604–1615 (2004).

    Article  CAS  Google Scholar 

  14. de Jonge, R. et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl Acad. Sci. USA 109, 5110–5115 (2012).

    Article  CAS  Google Scholar 

  15. 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  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Jehle, A. K. et al. The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25, 2330–2340 (2013).

    Article  CAS  Google Scholar 

  18. Du, J. et al. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants doi:10.1038/nplants.2015.34 (2015).

  19. 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  CAS  Google Scholar 

  20. Chinchilla, D., Shan, L., He, P., de Vries, S. & Kemmerling, B. One for all: the receptor-associated kinase BAK1. Trends Plant Sci. 14, 535–541 (2009).

    Article  CAS  Google Scholar 

  21. Bar, M., Sharfman, M., Ron, M. & Avni, A. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 63, 791–800 (2010).

    Article  CAS  Google Scholar 

  22. Fradin, E. F. et al. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156, 2255–2265 (2011).

    Article  CAS  Google Scholar 

  23. Gijzen, M. & Nürnberger, T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67, 1800–1807 (2006).

    Article  CAS  Google Scholar 

  24. Oome, S. & Van den Ackerveken, G. Comparative and functional analysis of the widely occurring family of nep1-like proteins. Mol. Plant Microbe Interact. 27, 1081–1094 (2014).

    Article  Google Scholar 

  25. Qutob, D. et al. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18, 3721–3744 (2006).

    Article  CAS  Google Scholar 

  26. Cabral, A. et al. Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis repression of necrosis-inducing activity by a surface-exposed region. Mol. Plant Microbe Interact. 25, 697–708 (2012).

    Article  CAS  Google Scholar 

  27. Dong, S. et al. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol. Plant Microbe Interact. 25, 896–909 (2012).

    Article  CAS  Google Scholar 

  28. Santhanam, P. et al. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant Microbe Interact. 26, 278–286 (2013).

    Article  CAS  Google Scholar 

  29. Böhm, H. et al. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. PLoS Pathog. 10, e1004491 (2014).

    Article  Google Scholar 

  30. Oome, S. et al. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 16955–16960 (2014).

    Article  CAS  Google Scholar 

  31. Postel, S. et al. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur. J. Cell Biol. 89, 169–174 (2010).

    Article  CAS  Google Scholar 

  32. Wang, G. et al. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 147, 503–5017 (2008).

    Article  CAS  Google Scholar 

  33. Jeworutzki, E. et al. Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels. Plant J. 62, 367–378 (2010).

    Article  CAS  Google Scholar 

  34. Krol, E. et al. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285, 13471–13479 (2010).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  36. 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  Google Scholar 

  37. Sun, Y. et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624–628 (2013).

    Article  CAS  Google Scholar 

  38. Haas, B. J. et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398 (2009).

    Article  CAS  Google Scholar 

  39. Jehle, A. K., Fürst, 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. Signal Behav. 8, pii: e27408 (2013).

    Article  Google Scholar 

  40. Lacombe, S. et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnol. 28, 365–369 (2010).

    Article  CAS  Google Scholar 

  41. Schoonbeek, H. J. et al. Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol. 206, 606–613 (2015).

    Article  CAS  Google Scholar 

  42. Afroz, A. et al. Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tiss. Organ Cult. 104, 227–237 (2010).

    Article  Google Scholar 

  43. 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  Google Scholar 

  44. Mendes, B. M. J. et al. Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol. 59, 68–75 (2010).

    Article  CAS  Google Scholar 

  45. Schwessinger, B. et al. Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLoS Pathog. 11, e1004809 (2015).

    Article  Google Scholar 

  46. Tripathi, J. N., Lorenzen, J., Bahar, O., Ronald, P. & Tripathi, L. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. muscearum. Plant Biotechnol. J. 12, 663–673 (2014).

    Article  CAS  Google Scholar 

  47. 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  Google Scholar 

  48. Gust, A. A., Brunner, F. & Nürnberger, T. Biotechnological concepts for improving plant innate immunity. Curr. Opin. Biotechnol. 21, 204–210 (2010).

    Article  CAS  Google Scholar 

  49. Monaghan, J. & Zipfel, C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349–357 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  51. Grefen, C. & Blatt, M. R. A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). BioTechniques 53, 311–314 (2012).

    Article  CAS  Google Scholar 

  52. McLellan, H. et al. An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathog. 9, e1003670 (2013).

    Article  Google Scholar 

  53. Llorente, B. et al. A quantitative real-time PCR method for in planta monitoring of Phytophthora infestans growth. Lett. Appl. Microbiol. 51, 603–610 (2010).

    Article  CAS  Google Scholar 

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Acknowledgements

Research in the laboratory of T.N. was funded by DFG grant Nu 70/9, funds of the University of Tübingen and SFB1101. Research in the G.V.d.A. laboratory was partly financed by a ‘more with less’ grant of the Netherlands Organization for Scientific Research. We are grateful to C. Oecking for critical discussions, to K. Berendzen for technical advice and to D. Chinchilla and J. Felix for providing an anti-SERK-antibody.

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Author notes

  1. Stan Oome

    Present address: †Present address: Averis Seeds BV, Valthermond, The Netherlands,

  2. Isabell Albert and Hannah Böhm: These authors contributed equally to this work.

Authors and Affiliations

  1. Center of Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 32, Tübingen, D-72076, Germany

    Isabell Albert, Hannah Böhm, Markus Albert, Christina E. Feiler, Julia Imkampe, Niklas Wallmeroth, Caterina Brancato, Christopher Grefen, Andrea A. Gust & Thorsten Nürnberger

  2. Department of Biology, Plant-Microbe Interactions, Utrecht University, Padualaan 8, Utrecht, 3584 CH, The Netherlands

    Tom M. Raaymakers, Stan Oome & Guido Van den Ackerveken

  3. Centre for BioSystems Genomics (CBSG), Wageningen, The Netherlands

    Stan Oome & Guido Van den Ackerveken

  4. Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China

    Heqiao Zhang & Jijie Chai

  5. Department of Plant Physiology and Biophysics, University of Würzburg, Julius-von-Sachs-Platz 2, Würzburg, D-97082, Germany

    Elzbieta Krol & Rainer Hedrich

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Contributions

T.N., G.V.d.A., J.C., R.H., I.A., H.B., M.A., J.I., S.O., T.M.R., C.G., A.A.G. and E.K. conceived and designed the experiments; I.A., H.B., M.A., C.F., J.I., N.W., C.G., T.M.R., H.Z. and E.K. conducted experiments and analysed data; C.B. produced transgenic plants; and I.A., H.B. and T.N. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Thorsten Nürnberger.

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Albert, I., Böhm, H., Albert, M. et al. An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nature Plants 1, 15140 (2015). https://doi.org/10.1038/nplants.2015.140

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