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CITRX thioredoxin interacts with the tomato Cf‐9 resistance protein and negatively regulates defence

Susana Rivas, Alejandra Rougon‐Cardoso, Matthew Smoker, Leif Schauser, Hirofumi Yoshioka, Jonathan D G Jones

Author Affiliations

  1. Susana Rivas,
  2. Alejandra Rougon‐Cardoso,
  3. Matthew Smoker,
  4. Leif Schauser,
  5. Hirofumi Yoshioka§ and
  6. Jonathan D G Jones*,1
  1. 1 The Sainsbury Laboratory, John Innes Centre, Norwich Research Park, Norwich, UK
  1. *Corresponding author. The Sainsbury Laboratory, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK. Tel.: +44 1603 452471; Fax: +44 1603 450011; E-mail: jonathan.jones{at}sainsbury-laboratory.ac.uk
  • Present address: Institut des Interactions Plantes‐Microorganismes, UMR CNRS/INRA, BP 27, Castanet‐Tolosan Cedex, France

  • Present address: Department of Computer Science, Bioinformatics Research Center, University of Aarhus, Ny Munkegade, Building 540, 8000 Århus C, Denmark

  • § Present address: Plant Pathology Laboratory, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464‐8601, Japan

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Abstract

To identify proteins involved in tomato Cf‐9 resistance protein function, a yeast two‐hybrid screen was undertaken using the cytoplasmic C‐terminus of Cf‐9 as bait. A thioredoxin‐homologous clone, interacting specifically with Cf‐9, was identified and called CITRX (Cf‐9‐interacting thioredoxin). Virus‐induced gene silencing (VIGS) of CITRX resulted in an accelerated Cf‐9/Avr9‐triggered hypersensitive response in both tomato and Nicotiana benthamiana, accompanied by enhanced accumulation of reactive oxygen species, alteration of protein kinase activity and induction of defence‐related genes. VIGS of CITRX also conferred increased resistance to the fungal pathogen Cladosporium fulvum in the otherwise susceptible Cf0 tomato. CITRX acts as a negative regulator of the cell death and defence responses induced through Cf‐9, but not Cf‐2. Recognition of the Cf‐9 C‐terminus by CITRX is necessary and sufficient for this negative regulation. This is the first study that implicates thioredoxin activity in the regulation of plant disease resistance.

  • Received February 10, 2004.
  • Accepted April 6, 2004.
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