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The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein

Nature Plants volume 2, Article number: 16185 (2016) Cite this article

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An Author Correction to this article was published on 23 October 2017

Abstract

Plants and animals recognize microbial invaders by detecting microbe-associated molecular patterns (MAMPs) by cell surface receptors. Many plant species of the Solanaceae family detect the highly conserved nucleic acid binding motif RNP-1 of bacterial cold-shock proteins (CSPs), represented by the peptide csp22, as a MAMP. Here, we exploited the natural variation in csp22 perception observed between cultivated tomato (Solanum lycopersicum) and Solanum pennellii to map and identify the leucine-rich repeat (LRR) receptor kinase CORE (cold shock protein receptor) of tomato as the specific, high-affinity receptor site for csp22. Corroborating its function as a genuine receptor, heterologous expression of CORE in Arabidopsis thaliana conferred full sensitivity to csp22 and, importantly, it also rendered these plants more resistant to infection by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Our study also confirms the biotechnological potential of enhancing plant immunity by interspecies transfer of highly effective pattern-recognition receptors such as CORE to different plant families.

Active defence against microbial pathogens depends on the detection of the infectious agents. As part of their innate immune system, plants use membrane-bound pattern-recognition receptors (PRRs) to detect a variety of MAMPs1. Most of the plant PRRs identified so far belong to the multi-membered protein families of receptor-like proteins (RLPs) and receptor-like kinases (RLKs)2–5. Although the number of RLKs and RLPs with functional attributions is steadily increasing6, the vast majority of these putative receptors remain orphan with respect to their biological functions and ligands. In turn, there is an increasing number of specific molecules that trigger responses in plant cells at nanomolar concentrations, indicating that they might act as ligands for as yet unidentified surface receptors. Matching such signals with their respective receptor proteins as ligand–receptor pairs remains a major task for plant research.

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Figure 1: Csp22-dependent induction of ethylene biosynthesis in tomato (S. lycopersicum), S. pennellii and a collection of recombinant inbred lines.
Figure 2: Csp22-dependent induction of MAMP responses in non-transformed N. benthamiana and in N. benthamiana expressing receptor candidate genes from tomato (S. lycopersicum).
Figure 3: CORE forms a complex with SERK3 in response to treatment with csp22 or csp15.
Figure 4: CORE binds csp22 and csp15 with high affinity and high specificity.
Figure 5: The receptor kinase CORE is sufficient to confer responsiveness to csp22 when expressed in cells of A. thaliana.
Figure 6: The receptor kinase CORE expressed in A. thaliana is fully functional and contributes to resistance against the bacterial pathogen Pseudomonas syringae pv. tomato strain DC3000 (Pst DC3000).

References

  1. 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  Google Scholar 

  2. Shiu, S. H. & Bleecker, A. B. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE 2001, re22 (2001).

  3. Shiu, S. H. et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220–1234 (2004).

    Article  CAS  Google Scholar 

  4. Wang, G. et al. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 147, 503–517 (2008).

    Article  CAS  Google Scholar 

  5. Fritz-Laylin, L. K., Krishnamurthy, N., Tor, M., Sjolander, K. V. & Jones, J. D. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol. 138, 611–623 (2005).

    Article  CAS  Google Scholar 

  6. Li, J. & Tax, F. E. Receptor-like kinases: key regulators of plant development and defense. J. Integr. Plant Biol. 55, 1184–1187 (2013).

    Article  CAS  Google Scholar 

  7. Felix, G. & Boller, T. Molecular sensing of bacteria in plants – the highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278, 6201–6208 (2003).

    Article  CAS  Google Scholar 

  8. Bae, W., Xia, B., Inouye, M. & Severinov, K. Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc. Natl Acad. Sci. USA 97, 7784–7789 (2000).

    Article  CAS  Google Scholar 

  9. Eshed, Y. & Zamir, D. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141, 1147–1162 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Chitwood, D. H. et al. A quantitative genetic basis for leaf morphology in a set of precisely defined tomato introgression lines. Plant Cell 25, 2465–2481 (2013).

    Article  CAS  Google Scholar 

  11. Bolger, A. et al. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat. Genet. 46, 1034–1038 (2014).

    Article  CAS  Google Scholar 

  12. Saur, I. M. et al. NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. Proc. Natl Acad. Sci. USA 113, 3389–3394 (2016).

    Article  CAS  Google Scholar 

  13. 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  Google Scholar 

  14. Clarke, C. R. et al. Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol. 200, 847–860 (2013).

    Article  CAS  Google Scholar 

  15. Thuerig, B., Felix, G., Binder, A., Boller, T. & Tamm, L. An extract of Penicillium chrysogenum elicits early defense-related responses and induces resistance in Arabidopsis thaliana independently of known signalling pathways. Physiol. Mol. Plant Pathol. 67, 180–193 (2005).

    Article  Google Scholar 

  16. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003).

    Article  CAS  Google Scholar 

  17. 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 

  18. Song, W. Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806 (1995).

    Article  CAS  Google Scholar 

  19. 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  Google Scholar 

  20. Bombarely, A. et al. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol. Plant Microbe Interact. 25, 1523–1530 (2012).

    Article  CAS  Google Scholar 

  21. 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 

  22. 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  Google Scholar 

  23. Butenko, M. A. et al. Tools and strategies to match peptide–ligand receptor pairs. Plant Cell 26, 1838–1847 (2014).

    Article  CAS  Google Scholar 

  24. Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572 (2007).

    Article  CAS  Google Scholar 

  25. Albert, M. et al. Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors. J. Biol. Chem. 285, 19035–19042 (2010).

    Article  CAS  Google Scholar 

  26. 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 

  27. Robatzek, S. et al. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 64, 539–547 (2007).

    Article  CAS  Google Scholar 

  28. Hind, S.R. et al. Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat. Plants 2, 16128 (2016).

    Article  CAS  Google Scholar 

  29. 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 

  30. Liu, X. K. et al. Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. eLife 3, e01990 (2014).

    Article  Google Scholar 

  31. Kunze, G. et al. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16, 3496–3507 (2004).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  33. Hegenauer, V. et al. Detection of the plant parasite Cuscuta reflexa by a tomato cell surface receptor. Science 353, 478–481 (2016).

    Article  CAS  Google Scholar 

  34. Gómez-Gómez, L., Felix, G. & Boller, T. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277–284 (1999).

    Article  Google Scholar 

  35. 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 Signal Behav. 8, e27408 (2013).

    Article  Google Scholar 

  36. 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 

  37. Albert, M. et al. Regulation of cell behaviour by plant receptor kinases: pattern recognition receptors as prototypical models. Eur. J. Cell Biol. 89, 200–207 (2010).

    Article  CAS  Google Scholar 

  38. Song, C., Kumar, A. & Saleh, M. Bioinformatic comparison of bacterial secretomes. Genomics Proteomics Bioinformatics 7, 37–46 (2009).

    Article  CAS  Google Scholar 

  39. Vazquez-Laslop, N., Lee, H., Hu, R. & Neyfakh, A. A. Molecular sieve mechanism of selective release of cytoplasmic proteins by osmotically shocked Escherichia coli. J. Bacteriol. 183, 2399–2404 (2001).

    Article  CAS  Google Scholar 

  40. Eshed, Y. & Zamir, D. Introgressions from Lycopersicon pennellii can improve the soluble-solids yield of tomato hybrids. Theor. Appl. Genet. 88, 891–897 (1994).

    Article  CAS  Google Scholar 

  41. 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 

Download references

Acknowledgements

The authors are grateful to I. Bock (Univ. Tübingen) for technical assistance, to H. Kalbacher (Univ. Tübingen) for helping with the synthesis of acri-csp22, to S. Robatzek (TSL, Norwich) for supplying SlSERK3a-myc and to J. Fliegmann (Univ. Tübingen) and D. Chinchilla (Univ. Basel) for critical reading of the manuscript. This work was supported by BMBF-KBBE project 031A328 and by Deutsche Forschungsgemeinschaft through CRC 1101.

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  1. ZMBP, University of Tübingen, Auf der Morgenstelle 32, D-72076 Tübingen, Germany

    Lei Wang, Markus Albert, Elias Einig, Ursula Fürst, Damaris Krust & Georg Felix

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  1. Lei Wang
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  2. Markus Albert
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Contributions

L.W., M.A., E.E., U.F., D.K. and G.F. performed experiments and analysed data; L.W., M.A. and G.F. designed experiments; L.W., M.A. and G.F. wrote the manuscript.

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Correspondence to Georg Felix.

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Supplementary Figures 1–6, Supplementary Table 1. (PDF 542 kb)

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Wang, L., Albert, M., Einig, E. et al. The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein. Nature Plants 2, 16185 (2016). https://doi.org/10.1038/nplants.2016.185

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