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First published online November 18, 2005; 10.1104/pp.105.070789

Plant Physiology 139:1795-1805 (2005)
© 2005 American Society of Plant Biologists

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Right arrow Reactive Oxygen Species
ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

The Alternative Oxidase of Plant Mitochondria Is Involved in the Acclimation of Shoot Growth at Low Temperature. A Study of Arabidopsis AOX1a Transgenic Plants1,[W]

Fabio Fiorani2, Ann L. Umbach* and James N. Siedow

Developmental, Cell, and Molecular Biology Group/Biology Department, Duke University, Durham, North Carolina 27708–1000

The alternative oxidase (AOX) pathway of plant mitochondria uncouples respiration from mitochondrial ATP production and may ameliorate plant performance under stressful environmental conditions, such as cold temperatures, by preventing excess accumulation of reactive oxygen species. We tested this model in whole tissues by growing AtAOX1a-transformed Arabidopsis (Arabidopsis thaliana) plants at 12°C. For the first time, to our knowledge, in plants genetically engineered for AOX, we identified a vegetative shoot growth phenotype. Compared with wild type at day 21 after sowing, anti-sense and overexpressing lines showed, on average, 27% reduced leaf area and 25% smaller rosettes versus 30% increased leaf area and 33% larger rosette size, respectively. Lines overexpressing a mutated, constitutively active AOX1a showed smaller phenotypic effects. These phenotypic differences were not the result of a major alteration of the tissue redox state because the changes in levels of lipid peroxidation products, reflecting oxidative damage, and the expression of genes encoding antioxidant and electron transfer chain redox enzymes did not correspond with the shoot phenotypes. However, the observed phenotypes were correlated with the amount of total shoot anthocyanin at low temperature and with the transcription of the flavonoid pathway genes PAL1 and CHS. These results demonstrate that (1) AOX activity plays a role in shoot acclimation to low temperature in Arabidopsis, and that (2) AOX not only functions to prevent excess reactive oxygen species formation in whole tissues under stressful environmental conditions but also affects metabolism through more pervasive effects, including some that are extramitochondrial.


1 This work was supported by the National Science Foundation (grant no. MCB–0091080 to J.N.S. and A.L.U.).

2 Present address: VIB-Ghent University, Plant Systems Biology, Technologiepark 927, B–9052 Ghent, Belgium.

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: Ann L. Umbach (umbacha{at}duke.edu).

[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.105.070789.

* Corresponding author; e-mail umbacha{at}duke.edu; fax 919–613–8177.

Received August 30, 2005; returned for revision October 18, 2005; accepted October 19, 2005.


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