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First published online April 7, 2006; 10.1104/pp.106.078469

Plant Physiology 141:423-435 (2006)
© 2006 American Society of Plant Biologists

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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 Tobacco1,[W]

Cristina Pignocchi2, Guy Kiddle, Iker Hernández3, Simon J. Foster2, Amparo Asensi, Tahar Taybi, Jeremy Barnes and Christine H. Foyer*

Crop Performance and Improvement Division (C.P., G.K., C.H.F.) and Plant Pathogen Interactions Division (S.J.F.), Rothamsted Research, Harpenden, Herts AL5 2JQ, United Kingdom; and Institute for Research on the Environment and Sustainability, School of Biology and Psychology, Division of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (I.H., A.A., T.T., J.B.)

The role of the redox state of the apoplast in hormone responses, signaling cascades, and gene expression was studied in transgenic tobacco (Nicotiana tabacum) plants with modified cell wall-localized ascorbate oxidase (AO). High AO activity specifically decreased the ascorbic acid (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 wild-type or AO antisense lines. Oxidation of apoplastic AA in AO sense lines was associated with loss of the auxin response, higher mitogen-activated protein 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 disulfide, 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 wild-type 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.

1 This work was supported by a combination of funding from the Biotechnology and Biological Sciences Research Council, the National Environmental Research Council, and the European Union (Marie Curie training site HPMT–CT–2001–00219).

2 Present address: The Sainsbury Laboratory, John Innes Centre, Norwich, Research Park NR4 7UH, UK.

3 Present address: Departament de Fisiologia Vegetal, Universitat de Barcelona, Avenida Diagona 645, 08028 Barcelona, Spain.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Christine H. Foyer (christine.foyer{at}bbsrc.ac.uk).

[W] The online version of this article contains Web-only data.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.078469.

* Corresponding author; e-mail christine.foyer{at}bbsrc.ac.uk; fax 44–1582–763010.

Received February 2, 2006; returned for revision March 24, 2006; accepted March 27, 2006.




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