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Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system

Nature Plants volume 2, Article number: 16128 (2016) Cite this article

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Abstract

Plants and animals detect the presence of potential pathogens through the perception of conserved microbial patterns by cell surface receptors. Certain solanaceous plants, including tomato, potato and pepper, detect flgII-28, a region of bacterial flagellin that is distinct from that perceived by the well-characterized FLAGELLIN-SENSING 2 receptor. Here we identify and characterize the receptor responsible for this recognition in tomato, called FLAGELLIN-SENSING 3. This receptor binds flgII-28 and enhances immune responses leading to a reduction in bacterial colonization of leaf tissues. Further characterization of FLS3 and its signalling pathway could provide new insights into the plant immune system and transfer of the receptor to other crop plants offers the potential of enhancing resistance to bacterial pathogens that have evolved to evade FLS2-mediated immunity.

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Figure 1: flgII-28 responsiveness is associated with one genomic region in tomato.
Figure 2: FLS3 is associated with enhanced resistance to bacterial infection.
Figure 3: FLS3 confers flgII-28 sensitivity.
Figure 4: FLS3 directly and specifically binds flgII-28.
Figure 5: FLS3 signalling is BAK1-dependent and is suppressed by effectors.

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Acknowledgements

We thank E. van der Knapp for providing tomato seeds, H.-L. Wei for DC3000 strains, J. Debbie for assistance with analysis of the FLS3 sequences from various tomato cultivars, C. Kraus and S. Schwizer for testing FLS3 expression in Arabidopsis thaliana, S. Schwizer and J. Mathieu for DNA constructs and S. Schwizer for proofreading. This research was supported by grants from the National Science Foundation to G.B.M. (IOS-1025642) and B.A.V. (IOS-1354215), the USDA-National Initiative in Food and Agriculture (2010-65108-20503) to G.B.M., the USDA Binational Agriculture Development Fund (IS-4931-16C) to G.B.M. and the National Institutes of Health (R01-GM078021) to G.B.M.; by the TRIAD foundation to G.B.M. and F.C.S.; by a Postdoctoral Fellowship from the Human Frontiers Science Program to P.C.B.; by a summer REU stipend to E.G.V. (National Science Foundation REU Site award DBI-1358843); and by internal funding from the Boyce Thompson Institute to S.R.S.

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Authors and Affiliations

  1. Boyce Thompson Institute for Plant Research, Ithaca, 14853, New York, USA

    Sarah R. Hind, Susan R. Strickler, Patrick C. Boyle, Diane M. Dunham, Zhilong Bao, Inish M. O'Doherty, Joshua A. Baccile, Jason S. Hoki, Elise G. Viox, Frank C. Schroeder & Gregory B. Martin

  2. Department of Chemistry and Chemical Biology, Cornell University, Ithaca, 14853, New York, USA

    Inish M. O'Doherty, Joshua A. Baccile, Jason S. Hoki & Frank C. Schroeder

  3. Department of Plant Pathology, Physiology and Weed Sciences, Virginia Tech, Blacksburg, 24061, Virginia, USA

    Christopher R. Clarke & Boris A. Vinatzer

  4. Section of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, 14853, New York, USA

    Gregory B. Martin

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Contributions

S.R.H. and G.B.M. conceived, designed and analysed experiments; S.R.H. performed the experiments except as noted below. S.R.S. designed and performed the bioinformatics analyses, and assisted with primer design. D.M.D. performed some of the experiments shown in Fig. 2 and Supplementary Figs 5, 6 and 8. P.C.B., I.M.O. and J.A.B. conceived and designed the experiments shown in Fig. 4 and Supplementary Fig. 7. Z.B. cloned, sequenced and analysed the FLS3 genomic sequences from tomato cultivars and S. pimpinellifolium accessions. E.G.V. performed the experiments shown in Fig. 2a,b. I.M.O., J.A.B. and F.C.S. provided technical assistance and advice in the development and application of crosslinking and click chemistry conditions, and I.M.O., J.A.B. and J.S.H. designed and synthesized the chemistries needed for the peptide probe generation. B.A.V. and C.R.C. designed and C.R.C. performed the experiments in Supplementary Fig. 1d–f. S.R.H. and G.B.M. wrote the manuscript with input from all co-authors.

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Correspondence to Gregory B. Martin.

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The authors declare no competing financial interests.

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Supplementary Figs 1–8, Supplementary Tables 1 and 2, Supplementary Methods and Materials, and Supplementary References. (PDF 2733 kb)

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Hind, S., Strickler, S., Boyle, P. et al. Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nature Plants 2, 16128 (2016). https://doi.org/10.1038/nplants.2016.128

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