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.
This is a preview of subscription content, access via your institution
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Macho, A. P. & Zipfel, C. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54, 263–272 (2014).
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).
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).
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).
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).
Dou, D. & Zhou, J. M. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484–495 (2012).
Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Rev. Genet. 11, 539–548 (2010).
Thomma, B. P., Nürnberger, T. & Joosten, M. H. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4–15 (2011).
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).
Zipfel, C. et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760 (2006).
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).
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).
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).
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).
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).
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).
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).
Du, J. et al. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants doi:10.1038/nplants.2015.34 (2015).
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).
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).
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).
Fradin, E. F. et al. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156, 2255–2265 (2011).
Gijzen, M. & Nürnberger, T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67, 1800–1807 (2006).
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).
Qutob, D. et al. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18, 3721–3744 (2006).
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).
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).
Santhanam, P. et al. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant Microbe Interact. 26, 278–286 (2013).
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).
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).
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).
Wang, G. et al. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 147, 503–5017 (2008).
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).
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).
Bi, G. et al. Arabidopsis thaliana receptor-like protein AtRLP23 associates with the receptor-like kinase AtSOBIR1. Plant Signal Behav. 9, e27937 (2014).
Santiago, J., Henzler, C. & Hothorn, M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341, 889–892 (2013).
Sun, Y. et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624–628 (2013).
Haas, B. J. et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398 (2009).
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).
Lacombe, S. et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnol. 28, 365–369 (2010).
Schoonbeek, H. J. et al. Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol. 206, 606–613 (2015).
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).
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).
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).
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).
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).
Dangl, J. L., Horvath, D. M. & Staskawicz, B. J. Pivoting the plant immune system from dissection to deployment. Science 341, 746–751 (2013).
Gust, A. A., Brunner, F. & Nürnberger, T. Biotechnological concepts for improving plant innate immunity. Curr. Opin. Biotechnol. 21, 204–210 (2010).
Monaghan, J. & Zipfel, C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349–357 (2012).
Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007).
Grefen, C. & Blatt, M. R. A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). BioTechniques 53, 311–314 (2012).
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).
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).
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.
The authors declare no competing financial interests.
About this article
Cite this article
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
This article is cited by
A glycoside hydrolase 12 protein from Cytospora chrysosperma triggers plant immunity but is not essential to virulence
Phytopathology Research (2023)
Convergent evolution of plant pattern recognition receptors sensing cysteine-rich patterns from three microbial kingdoms
Nature Communications (2023)
The COG1-OsSERL2 complex senses cold to trigger signaling network for chilling tolerance in japonica rice
Nature Communications (2023)
Stress Biology (2023)
Journal of Plant Biology (2023)