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OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis

Nature volume 427, pages 858–861 (2004)Cite this article

Abstract

Active oxygen species (AOS) generated in response to stimuli and during development can function as signalling molecules in eukaryotes, leading to specific downstream responses1,2. In plants these include such diverse processes as coping with stress (for example pathogen attack3, wounding4 and oxygen deprivation5), abscisic-acid-induced guard-cell closure6, and cellular development (for example root hair growth7). Despite the importance of signalling via AOS in eukaryotes, little is known about the protein components operating downstream of AOS that mediate any of these processes. Here we show that expression of an Arabidopsis thaliana gene (OXI1) encoding a serine/threonine kinase is induced in response to a wide range of H2O2-generating stimuli. OXI1 kinase activity is itself also induced by H2O2 in vivo. OXI1 is required for full activation of the mitogen-activated protein kinases (MAPKs) MPK3 and MPK6 after treatment with AOS or elicitor and is necessary for at least two very different AOS-mediated processes: basal resistance to Peronospora parasitica infection, and root hair growth. Thus, OXI1 is an essential part of the signal transduction pathway linking oxidative burst signals to diverse downstream responses.

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Figure 1: H2O2, cellulase and wounding increase the expression of OXI1.
Figure 2: OXI1 is necessary for basal resistance to P. parasitica.
Figure 3: OXI1 is necessary for normal root hair development.
Figure 4: OXI1 kinase activity is induced by H2O2 and cellulase, and OXI1 is necessary for MPK3 and MPK6 activation.

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Acknowledgements

We thank A. Rehmany for the P. parasitica isolates; A. Hailey for statistical analysis; B. Ellis and G. Miles for discussions; and N. Evans, S. Gurr and R. Capper and K. Denby for practical and moral support. This work was funded by the BBSRC, the Gatsby Foundation, the EU TMR program, the Cannon Collins Educational Trust for Southern Africa (CCETSA), the South African National Research Foundation (NRF), and the Austrian Science Foundation.

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Author notes

  1. Maike C. Rentel

    Present address: Department of Cellular and Molecular Pharmacology, University of California, San Francisco, California, 94143-0450, USA

Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, OX1 3RB, Oxford, UK

    Maike C. Rentel, Lindsay Petersen, Haruko Okamoto, Heather Knight & Marc R. Knight

  2. Max F. Perutz Laboratories of the University of Vienna and Gregor-Mendel-Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna Biocenter, 1030, Vienna, Austria

    David Lecourieux, Fatma Ouaked & Heribert Hirt

  3. School of Biological Sciences, University of Bristol, BS8 1UG, Bristol, UK

    Sarah L. Usher & Claire S. Grierson

  4. Department of Molecular and Cell Biology, University of Cape Town, Private Bag Rondebosch 7701, South Africa

    Lindsay Petersen

  5. Sainsbury Laboratory, NR4 7UH, Norwich, UK

    Scott C. Peck

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Correspondence to Maike C. Rentel or Heribert Hirt.

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Supplementary information

Supplementary Figure 1

Plants containing an OXI1::GUS gene construct were wounded with tweezers and stained for (a) H2O2 production with diaminobenzidine (DAB) or (b) expression of the GUS protein24. (PDF 236 kb)

Supplementary Figure 2

Low magnification (top) and higher magnification (bottom) of roots grown on (a) ordinary agar and (b) phytagel. (PDF 132 kb)

Supplementary Figure 3

Distribution of mature root hair lengths of (a) oxi1 and Ws-2 seedlings and (b) oxi1 and complemented oxi1 seedlings (oxi1 + OXI1) with roots growing through air. (PDF 45 kb)

Supplementary Figure Legends (DOC 19 kb)

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Rentel, M., Lecourieux, D., Ouaked, F. et al. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861 (2004). https://doi.org/10.1038/nature02353

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