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Perception of Agrobacterium tumefaciens flagellin by FLS2XL confers resistance to crown gall disease

Abstract

Bacterial flagella are perceived by the innate immune systems of plants1 and animals2 alike, triggering resistance. Common to higher plants is the immunoreceptor FLAGELLIN-SENSING 2 (FLS2)3, which detects flagellin via its most conserved epitope, flg22. Agrobacterium tumefaciens, which causes crown gall disease in many crop plants, has a highly diverged flg22 epitope and evades immunodetection by plants so far studied. We asked whether, as a next step in this game of ‘hide and seek’, there are plant species that have evolved immunoreceptors with specificity for the camouflaged flg22Atum of A. tumefaciens. In the wild grape species Vitis riparia, we discovered FLS2XL, a previously unknown form of FLS2, that provides exquisite sensitivity to typical flg22 and to flg22Atum. As exemplified by ectopic expression in tobacco, FLS2XL can limit crown gall disease caused by A. tumefaciens.

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Fig. 1: Vitis riparia cell cultures respond to flg22 and flg22Atum with extracellular alkalinization.
Fig. 2: FLS2XL perceives flg22Atum at subnanomolar concentrations.
Fig. 3: FLS2XL exhibits similar affinity for flg22 and flg22Atum.
Fig. 4: FLS2XL renders N. tabacum more resistant to A. tumefaciens.

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Data availability

All data are available in the main text or the supplementary materials.

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Acknowledgements

We thank I. Bock, P. Neumann and C. Brancato (ZMBP, Tübingen) for maintenance of plant cells and help with plant transformation, H. Kalbacher (University of Tübingen) for peptide modification and R. Fuchs and H.-H. Kassemeyer, Staatliches Weinbauinstitut, Freiburg, Germany for providing the cell culture of V. riparia. We are grateful for financial support from the German Federal Ministry of Education (BMBF-KBBE project No. 031A328 36) to U.F., and from the Deutsche Forschungsgemeinschaft (grant no. DFG-CRC1101) to J.F. and G.F., and (grant no. DFG/AL1426/1–2) to M.A.

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U.F., M.A. and G.F. designed the study, supervised experiments and analysed data. U.F. performed most of the experimental work and wrote the draft of the manuscript. Y.Z. performed the initial screen for plants with sensitivity to flg22Atum. M.A., A.K.W., J.F. and G.F. provided expertise and practical support for cloning, expression and functional analysis of FLS2 receptors. All authors contributed to the manuscript.

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Correspondence to Georg Felix.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Jijie Chai, Pamela Ronald and Ive de Smet for their contribution to the peer review of this work.

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Supplementary Figs. 1–6, Supplementary Table 1 and Supplementary Reference.

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Fürst, U., Zeng, Y., Albert, M. et al. Perception of Agrobacterium tumefaciens flagellin by FLS2XL confers resistance to crown gall disease. Nat. Plants 6, 22–27 (2020). https://doi.org/10.1038/s41477-019-0578-6

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