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.

  • Letter
  • Published:

The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects

Nature Plants volume 4, pages 152–156 (2018)Cite this article

Subjects

Abstract

The discovery in tomato of systemin, the first plant peptide hormone1,2, was a fundamental change for the concept of plant hormones. Numerous other peptides have since been shown to play regulatory roles in many aspects of the plant life, including growth, development, fertilization and interactions with symbiotic organisms3,4,5,6. Systemin, an 18 amino acid peptide derived from a larger precursor protein7, was proposed to act as the spreading signal that triggers systemic defence responses observed in plants after wounding or attack by herbivores1,7,8. Further work culminated in the identification of a leucine-rich repeat receptor kinase (LRR-RK) as the systemin receptor 160 (SR160)9,10. SR160 is a tomato homologue of Brassinosteroid Insensitive 1 (BRI1), which mediates the regulation of growth and development in response to the steroid hormone brassinolide11,12,13. However, a role of SR160/BRI1 as systemin receptor could not be corroborated by others14,15,16. Here, we demonstrate that perception of systemin depends on a pair of distinct LRR-RKs termed SYR1 and SYR2. SYR1 acts as a genuine systemin receptor that binds systemin with high affinity and specificity. Further, we show that presence of SYR1, although not decisive for local and systemic wound responses, is important for defence against insect herbivory.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The tomato genes SYR1/Solyc03g082470 and SYR2/Solyc03g082450 provide responsiveness to systemin when heterologously expressed in N. benthamiana or A. thaliana.
Fig. 2: SYR1 binds systemin with high affinity and specificity.
Fig. 3: Systemin perception is not essential for wound responses but contributes significantly to resistance against herbivory by insect larvae of S. littoralis.

Similar content being viewed by others

References

  1. Pearce, G., Strydom, D., Johnson, S. & Ryan, C. A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895–898 (1991).

    Article  CAS  PubMed  Google Scholar 

  2. Ryan, C. A. & Pearce, G. Systemin: a polypeptide signal for plant defensive genes. Annu. Rev. Cell. Dev. Biol. 14, 1–17 (1998).

    Article  CAS  PubMed  Google Scholar 

  3. Tavormina, P., De Coninck, B., Nikonorova, N., De Smet, I. & Cammue, B. P. A. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27, 2095–2118 (2015).

  4. Breiden, M. & Simon, R. Q&A: how does peptide signaling direct plant development? BMC Biol. 14, 58 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Matsubayashi, Y. & Sakagami, Y. Peptide hormones in plants. Annu. Rev. Plant Biol. 57, 649–674 (2006).

    Article  CAS  PubMed  Google Scholar 

  6. Matsubayashi, Y. Posttranslationally modified small-peptide signals in plants. Annu. Rev. Plant Biol. 65, 385–413 (2014).

    Article  PubMed  Google Scholar 

  7. McGurl, B. & Ryan, C. A. The organization of the prosystemin gene. Plant Mol. Biol. 20, 405–409 (1992).

    Article  CAS  PubMed  Google Scholar 

  8. McGurl, B., Pearce, G., Orozco-Cardenas, M. & Ryan, C. A. Structure, expression, and antisense inhibiton of the systemin precursor gene. Science 255, 1570–1573 (1992).

    Article  CAS  PubMed  Google Scholar 

  9. Scheer, J. M. & Ryan, C. A. The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc. Natl Acad. Sci. USA 99, 9585–9590 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Scheer, J. M., Pearce, G. & Ryan, C. A. Generation of systemin signaling in tobacco by transformation with the tomato systemin receptor kinase gene. Proc. Natl Acad. Sci. USA 100, 10114–10117 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kinoshita, T. et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167–171 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. She, J. et al. Structural insight into brassinosteroid perception by BRI1. Nature 474, 472–476 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hothorn, M. et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474, 467–471 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Holton, N. et al. Tomato BRASSINOSTEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling. Plant Cell. 19, 1709–1717 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Lanfermeijer, F. C., Staal, M., Malinowski, R., Stratmann, J. W. & Elzenga, J. T. Micro-electrode flux estimation confirms that the Solanum pimpinellifolium cu3 mutant still responds to systemin. Plant Physiol. 146, 129–139 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Malinowski, R. et al. The tomato brassinosteroid receptor BRI1 increases binding of systemin to tobacco plasma membranes, but is not involved in systemin signaling. Plant Mol. Biol. 70, 603–616 (2009).

    Article  CAS  PubMed  Google Scholar 

  17. Felix, G. & Boller, T. Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J. 7, 381–389 (1995).

  18. Ryan, C. A. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477, 112–121 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. 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).

  20. 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).

  21. Wang, L. et al. The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein. Nat. Plants 2, 16185 (2016).

    Article  CAS  PubMed  Google Scholar 

  22. 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).

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

    Article  CAS  PubMed  Google Scholar 

  24. Constabel, C. P., Yip, L. & Ryan, C. A. Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 36, 55–62 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Yamaguchi, Y., Pearce, G. & Ryan, C. A. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl Acad. Sci. USA 103, 10104–10109 (2006).

  26. Lori, M. et al. Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: interfamily incompatibility of perception but compatibility of downstream signalling. J. Exp. Bot. 66, 5315–5325 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  28. Meindl, T., Boller, T. & Felix, G. The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10, 1561–1570 (1998).

  29. Pearce, G., Johnson, S. & Ryan, C. A. Structure-activity of deleted and substituted systemin, an 18-amino acid polypeptide inducer of plant defensive genes. J. Biol. Chem. 268, 212–216 (1993).

    CAS  PubMed  Google Scholar 

  30. Malone, M., Alarcon, J. J. & Palumbo, L. A hydraulic interpretation of rapid, long-distance wound signalling in the tomato. Planta 193, 181–185 (1994).

    Article  CAS  Google Scholar 

  31. Wildon, D. C. et al. Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 62–65 (1992).

    Article  CAS  Google Scholar 

  32. Li, L., Li, C., Lee, G. I. & Howe, G. A. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc. Natl Acad. Sci. USA 99, 6416–6421 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mousavi, S. A., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422–426 (2013).

    Article  CAS  PubMed  Google Scholar 

  34. Zimmermann, M. R., Maischak, H., Mithofer, A., Boland, W. & Felle, H. H. System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol. 149, 1593–1600 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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  CAS  PubMed  PubMed Central  Google Scholar 

  36. Orozco-Cardenas, M., McGurl, B. & Ryan, C. A. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl Acad. Sci. USA 90, 8273–8276 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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).

  38. Van Eck, J., Kirk, D. D. & Walmsley, A. M. Tomato (Lycopersicum esculentum). Methods Mol. Biol. 343, 459–473 (2006).

    PubMed  Google Scholar 

  39. Maffei, M., Bossi, S., Spiteller, D., Mithofer, A. & Boland, W. Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol. 134, 1752–1762 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank I. Bock and C. Brancato (Tübingen) for technical assistance and T. Boller (Basel) for critical reading of the manuscript. We are grateful for financial support to L.W. and G.F. by DFG-CRC1101-D05 and to M.A. by DFG AL1426/1-2.

Author information

Authors and Affiliations

  1. The Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany

    Lei Wang, Elias Einig, Markus Albert, Judith Fliegmann & Georg Felix

  2. Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, Jena, Germany

    Marilia Almeida-Trapp & Axel Mithöfer

  3. Interfaculty Institute of Biochemistry, University of Tübingen, Tübingen, Germany

    Hubert Kalbacher

Authors
  1. Lei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elias Einig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marilia Almeida-Trapp
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Markus Albert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Judith Fliegmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Axel Mithöfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hubert Kalbacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Georg Felix
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.W. was involved in designing, performing and analysing of all experiments. H.K. synthesized the acridinium- and biotin-labelled peptides, M.A. contributed to ligand binding experiments in Fig. 2, E.E. to experiments in Fig. 3a,b,c and M.A.-T. and A.M. to experiments with insect larvae in Fig. 3d. L.W., J.F. and G.F. supervised the work, planned the experiments and wrote the manuscript.

Corresponding author

Correspondence to Georg Felix.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–7, Supplementary Tables 1 and 2.

Life Sciences Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Einig, E., Almeida-Trapp, M. et al. The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nature Plants 4, 152–156 (2018). https://doi.org/10.1038/s41477-018-0106-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0106-0

This article is cited by

Search

Advanced 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