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Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase

Nature Chemical Biology volume 10, pages 450–456 (2014)Cite this article

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Abstract

Specific chemicals can prime the plant immune system for augmented defense. β-aminobutyric acid (BABA) is a priming agent that provides broad-spectrum disease protection. However, BABA also suppresses plant growth when applied in high doses, which has hampered its application as a crop defense activator. Here we describe a mutant of Arabidopsis thaliana that is impaired in BABA-induced disease immunity (ibi1) but is hypersensitive to BABA-induced growth repression. IBI1 encodes an aspartyl-tRNA synthetase. Enantiomer-specific binding of the R enantiomer of BABA to IBI1 primed the protein for noncanonical defense signaling in the cytoplasm after pathogen attack. This priming was associated with aspartic acid accumulation and tRNA-induced phosphorylation of translation initiation factor eIF2α. However, mutation of eIF2α-phosphorylating GCN2 kinase did not affect BABA-induced immunity but relieved BABA-induced growth repression. Hence, BABA-activated IBI1 controls plant immunity and growth via separate pathways. Our results open new opportunities to separate broad-spectrum disease resistance from the associated costs on plant growth.

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Figure 1: Identification and characterization of the Arabidopsis ibi1 mutant.
Figure 2: Characterization of the defense function of IBI1.
Figure 3: Enantiomer-specific activity of BABA to IBI1.
Figure 4: BABA interferes with canonical AspRS activity.
Figure 5: Genetic separation of BABA-IR and growth repression.
Figure 6: The BABA receptor IBI1 controls BABA-IR and plant growth suppression via separate pathways.

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Acknowledgements

We thank S. van Wees, N. Halford, J. Lucas, J. Pickett, I. Feussner, X. Zhang, W. Kegge, D. Acoska, M. Roberts, V. Pastor, J. Gamir and B. Mauch-Mani for fruitful discussions, practical assistance and/or helpful feedback. Arabidopsis NahG B15 and Ler rpp5 seeds were kindly provided by J. Ryals (Research Triangle Park, USA) and J. Parker (Max Planck Institute, Cologne), respectively. The research was supported by a VENI grant to J.T. (no. 863.04.019) from the Netherlands Organisation of Scientific Research (NWO), a Biotechnology and Biological Sciences Research Council Institute Career Path Fellowship (no. BB/E023959/1) to J.T., a consolidator grant from the European Research Council (no. 309944-Prime-A-Plant) to J.T., a Research Leadership Award from the Leverhulme Trust (no. RL-2012-042) to J.T., European Union Seventh Framework Programme (FP7/2007-2013; n°265865-PURE) to J.T., a grant from the Felix Thornley Cobbold Agricultural Trust to J.T. and E.L. and a VICI grant (no. 865.04.002) to C.M.J.P. from NWO.

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Author notes

  1. Yuhua Zhang & Allison van de Meene

    Present address: Present addresses: Research and Development Center, Firmenich Aromatics (China) Co. Ltd., Shanghai, China (Y.Z.); School of Botany, The University of Melbourne, Victoria, Australia (A.v.d.M.).,

Authors and Affiliations

  1. Department of Animal and Plant Sciences, The University of Sheffield, Sheffield, UK

    Estrella Luna, Ana López, Pierre Pétriacq, Mike Burrell & Jurriaan Ton

  2. Rothamsted Research, Harpenden, UK

    Estrella Luna, Yuhua Zhang, Allison van de Meene & Jurriaan Ton

  3. Department of Biology, Utrecht University, Utrecht, The Netherlands

    Marieke van Hulten, Corné M J Pieterse & Jurriaan Ton

  4. Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia

    Oliver Berkowitz

  5. School of Plant Biology, University of Western Australia, Perth, Australia

    Oliver Berkowitz

  6. Department of Chemistry, University of Sheffield, Sheffield, UK

    Matthew A Sellwood & Beining Chen

  7. Departmento de Ciencias Agrarias y del Medio Ambiente, University of Jaume I, Castellon, Spain

    Victor Flors

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Contributions

J.T. designed and supervised the research plan, performed experiments (mutant screen, map-based cloning, construction of transgenic lines, RT-qPCR and bioassays) and wrote the manuscript. E.L. performed experiments (map-based cloning, construction of transgenic lines, RT-qPCR, bioassays, confocal microscopy and IP assays), wrote the manuscript and provided intellectual input. M.v.H. performed experiments (mutant screen and bioassays) and provided intellectual input. Y.Z. performed experiments (map-based cloning and RT-qPCR) and provided intellectual input. O.B. performed experiments (GCN2 activity assays) and provided intellectual input. A.L. performed experiments (confocal microscopy and IP assays). P.P. performed experiments (MS). M.A.S. did computational modeling. B.C. did computational modeling and provided intellectual input. M.B. provided intellectual input. A.v.d.M. performed experiments (confocal microscopy). C.M.J.P. provided intellectual input. V.F. performed experiments (bioassays) and provided intellectual input.

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Correspondence to Jurriaan Ton.

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Luna, E., van Hulten, M., Zhang, Y. et al. Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10, 450–456 (2014). https://doi.org/10.1038/nchembio.1520

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