Plant Physiology Preview
Published on April 7, 2006; 10.1104/pp.106.078469
Received February 2, 2006
Returned for revision February 25, 2006
Accepted March 27, 2006
Ascorbate-oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco
Cristina Pignocchi , Guy Kiddle , Iker Hernández , Simon J Foster , Amparo Asensi , Tahar Taybi , Jeremy Barnes , and Christine H. Foyer *
Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts, AL5 2JQ, U.K.
Institute for Research on the Environment and Sustainability, School of Biology and Psychology: Division of Biology, Devonshire Building, Newcastle University, Newcastle Upon Tyne NE1 7RU, U.K.
Plant Pathogen Interactions Division, Rothamsted Research, Harpenden, Herts, AL5 2JQ, U.K.
* Corresponding author; email: christine.foyer{at}bbsrc.ac.uk.
The role of the redox state of the apoplast on hormone responses, signaling cascades and gene expression was studied in transgenic tobacco plants with modified cell wall-localized ascorbate oxidase (AO). High AO activity specifically decreased the ascorbate (AA) content of the apoplast and altered plant growth responses triggered by hormones. Auxin stimulated shoot growth only when the apoplastic AA pool was reduced in the wild type (WT) or AO antisense lines. Oxidation of apoplastic AA in AO sense lines was associated with loss of the auxin response, higher MAP kinase activities and susceptibility to a virulent strain of the pathogen Pseudomonas syringae. The total leaf glutathione pool, the ratio of reduced glutathione to glutathione disulphide and glutathione reductase activities were similar in the leaves of all lines. However, AO sense leaves exhibited significantly lower dehydroascorbate reductase and ascorbate peroxidase activities than WT and antisense leaves. The abundance of mRNAs encoding antioxidant enzymes was similar in all lines. However, the day/night rhythms in the abundance of transcripts encoding the three catalase isoforms were changed in response to the AA content of the apoplast. Other transcripts influenced by AO included photorespiratory genes and a plasma membrane Ca2+ channel-associated gene. We conclude that the redox state of the apoplast modulates plant growth and defense responses by regulating signal transduction cascades and gene expression patterns. Hence AO activity, which modulates the redox state of the apoplastic AA pool, strongly influences the responses of plant cells to external and internal stimuli.
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