Article | Published:

GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling

Nature volume 500, pages 422426 (22 August 2013) | Download Citation

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Abstract

Wounded leaves communicate their damage status to one another through a poorly understood process of long-distance signalling. This stimulates the distal production of jasmonates, potent regulators of defence responses. Using non-invasive electrodes we mapped surface potential changes in Arabidopsis thaliana after wounding leaf eight and found that membrane depolarizations correlated with jasmonate signalling domains in undamaged leaves. Furthermore, current injection elicited jasmonoyl-isoleucine accumulation, resulting in a transcriptome enriched in RNAs encoding key jasmonate signalling regulators. From among 34 screened membrane protein mutant lines, mutations in several clade 3 GLUTAMATE RECEPTOR-LIKE genes (GLRs 3.2, 3.3 and 3.6) attenuated wound-induced surface potential changes. Jasmonate-response gene expression in leaves distal to wounds was reduced in a glr3.3 glr3.6 double mutant. This work provides a genetic basis for investigating mechanisms of long-distance wound signalling in plants and indicates that plant genes related to those important for synaptic activity in animals function in organ-to-organ wound signalling.

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Gene Expression Omnibus

Data deposits

Gene expression data are available in the GEO database under accession number GSE41779.

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Acknowledgements

Supported by a Faculty of Biology and Medicine Interdisciplinary grant (to S.K. and E.E.F.) and Swiss NSF grants 3100A0-122441 and 31003A-138235 (to E.E.F.). We thank I. Acosta, D. Gasperini, S. Stolz and A. Chételat and other Farmer lab members for critical comments and/or technical help, M. Blanchard for help with electrophysiology, and the Lausanne Genomic Technologies Facility and M. Shakhsi-Niaei for help with transcriptome analyses. We thank Y. Lee and F. Mauch for rbohD seeds, P. Schweizer and P. Reymond for insect larvae, J.-L. Wolfender for analytics support, and R. Benton, C. Fankhauser, N. Geldner, C. Hardtke and Y. Poirier for valuable comments.

Author information

Affiliations

  1. Department of Plant Molecular Biology, University of Lausanne, Biophore, CH-1015 Lausanne, Switzerland

    • Seyed A. R. Mousavi
    •  & Edward E. Farmer
  2. School of Pharmaceutical Sciences, University of Geneva, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland

    • Adeline Chauvin
  3. Department of Pharmacology and Toxicology, University of Lausanne, Rue du Bugnon 27, CH-1005 Lausanne, Switzerland

    • François Pascaud
    •  & Stephan Kellenberger

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Contributions

S.A.R.M., A.C., F.P. and S.K. performed experiments; E.E.F., S.A.R.M. and S.K. conceived experiments; E.E.F. and S.K. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Edward E. Farmer.

Extended data

Supplementary information

Excel files

  1. 1.

    Supplementary Data

    Gene expression in response to current injection or wounding: The file contains a list of genes that were upregulated more than 2-fold (P ≤ 0.05) in leaf 8 1h after injecting current into leaf 8 (this study), in leaf 13 1h after wounding leaf 8 (this study), and in wounded leaves of 18 d-old plants 1 h after wound infliction32, FC=fold change (upregulated), ci = current injection, no ci = no current injection.

Videos

  1. 1.

    Insect-induced electrical activity in Arabidopsis.

    Three Spodoptera littoralis larvae were placed on leaf 8 of a 5 week-old plant within a ring barrier. Surface potentials measured at the two electrodes are shown. A clock is displayed at upper right. The x-axis in ms and the y-axis is in V. Note that events that are recorded at the proximal electrode precede those recorded at the distal electrode and that the signal recorded at the distal electrode is simpler that at the proximal electrode. The video has been edited to shorten it.

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DOI

https://doi.org/10.1038/nature12478

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