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Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance

Nature Biotechnology volume 28, pages 365–369 (2010)Cite this article

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Abstract

Plant diseases cause massive losses in agriculture. Increasing the natural defenses of plants may reduce the impact of phytopathogens on agricultural productivity. Pattern-recognition receptors (PRRs) detect microbes by recognizing conserved pathogen-associated molecular patterns (PAMPs)1,2,3. Although the overall importance of PAMP-triggered immunity for plant defense is established2,3, it has not been used to confer disease resistance in crops. We report that activity of a PRR is retained after its transfer between two plant families. Expression of EFR (ref. 4), a PRR from the cruciferous plant Arabidopsis thaliana, confers responsiveness to bacterial elongation factor Tu in the solanaceous plants Nicotiana benthamiana and tomato (Solanum lycopersicum), making them more resistant to a range of phytopathogenic bacteria from different genera. Our results in controlled laboratory conditions suggest that heterologous expression of PAMP recognition systems could be used to engineer broad-spectrum disease resistance to important bacterial pathogens, potentially enabling more durable and sustainable resistance in the field.

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Figure 1: Eliciting activities of elf18 peptides and EF-Tu from selected phytopathogenic bacteria in A. thaliana.
Figure 2: Transgenic expression of EFR in N. benthamiana and tomato confers elf18 responsiveness.
Figure 3: Transgenic expression of EFR in N. benthamiana confers broad-spectrum bacterial resistance.
Figure 4: Transgenic expression of EFR in tomato confers broad-spectrum bacterial resistance.

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Acknowledgements

We thank the John Innes Centre Horticultural Services for great plant care; D. Studholme (The Sainsbury Laboratory) for providing the EF-Tu sequence from X. campestris pv. musacearum 4381; S. Humphris, L. Pritchard, P. Birch and I. Toth (Scottish Crop Research Institute) for providing the EF-Tu sequences and extracts from Dickeya dianthicola 3534, P. atrosepticum 1043 and P. carotovorum 193; B. Vinatzer (Virginia Tech), J. Rathjen (The Sainsbury Laboratory) and S. Gelvin (Purdue University) for providing cultures of Pss B728a, Pta 11528 and A. tumefaciens A281, respectively; and S. Kamoun, E. Ward and J. Rathjen for their critical reading of the manuscript. This work was funded by the Two Blades Foundation and the Gatsby Charitable Foundation. B.P.H.J.T. is supported by a Vidi grant of the Research Council for Earth and Life Sciences of the Netherlands Organization for Scientific Research and by European Research Area Networks Plant Genomics. The Two Blades Foundation has filed a patent on behalf of inventors J.D.G.J. and C.Z. on the use of EFR to confer broad-spectrum disease resistance in plants.

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Author notes

  1. Séverine Lacombe, Alejandra Rougon-Cardoso & Emma Sherwood

    Present address: Present addresses: Institut National de la Recherche Agronomique, Unité de Recherche, Génétique et Amélioration des Fruits et Légumes, Montfavet, France (S.L.), Laboratorio Nacional de Genómica para la Biodiversidad, CINVESTAV Irapuato, Irapuato, Mexico (A.R.-C.) and Department of Molecular Microbiology, John Innes Centre, Norwich, UK (E.S.).,

  2. Séverine Lacombe, Alejandra Rougon-Cardoso and Emma Sherwood: These authors contributed equally to this work.

Authors and Affiliations

  1. The Sainsbury Laboratory, Norwich Research Park, Norwich, UK

    Séverine Lacombe, Alejandra Rougon-Cardoso, Emma Sherwood, Matthew Smoker, Ghanasyam Rallapalli, Jonathan D G Jones & Cyril Zipfel

  2. Centre National de la Recherche Scientifique-Institut National de la Recherche Agronomique, Unité Mixte de Recherche, Laboratoire des Interactions Plantes Microorganismes, Castanet-Tolosan, France

    Nemo Peeters

  3. Department of Plant and Microbial Biology, University of California, Berkeley, California, USA

    Douglas Dahlbeck & Brian Staskawicz

  4. Laboratory of Phytopathology, Wageningen University, Wageningen, The Netherlands

    H Peter van Esse & Bart P H J Thomma

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  1. Séverine Lacombe
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Contributions

S.L., A.R.-C., E.S., N.P., D.D., H.P.E. and G.R. performed experiments and analyzed data. M.S. generated the transgenic plants. B.S. and B.P.H.J.T. contributed ideas, conceived experiments and analyzed data. J.D.G.J. initiated the project and contributed ideas. C.Z. initiated the project, conceived, designed and performed experiments, analyzed data, obtained funding, and wrote the manuscript. All authors commented on the manuscript prior to submission.

Corresponding author

Correspondence to Cyril Zipfel.

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The authors declare no competing financial interests.

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Lacombe, S., Rougon-Cardoso, A., Sherwood, E. et al. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28, 365–369 (2010). https://doi.org/10.1038/nbt.1613

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