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J. Biol. Chem., Vol. 282, Issue 49, 35749-35756, December 7, 2007

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Genetic Removal of Tri-unsaturated Fatty Acids Suppresses Developmental and Molecular Phenotypes of an Arabidopsis Tocopherol-deficient Mutant

WHOLE-BODY MAPPING OF MALONDIALDEHYDE POOLS IN A COMPLEX EUKARYOTE^*

Laurent Mène-Saffrané¹, Céline Davoine, Stéphanie Stolz, Paul Majcherczyk, and Edward E. Farmer²

From the Departments of Plant Molecular Biology and Fundamental Microbiology, University of Lausanne, Batîment Biophore, 1015 Lausanne, Switzerland

Malondialdehyde (MDA) is a small, ubiquitous, and potentially toxic aldehyde that is produced in vivo by lipid oxidation and that is able to affect gene expression. Tocopherol deficiency in the vitamin E2 mutant vte2-1 of Arabidopsis thaliana leads to massive lipid oxidation and MDA accumulation shortly after germination. MDA accumulation correlates with a strong visual phenotype (growth reduction, cotyledon bleaching) and aberrant GST1 (glutathione S-transferase 1) expression. We suppressed MDA accumulation in the vte2-1 background by genetically removing tri-unsaturated fatty acids. The resulting quadruple mutant, fad3-2 fad7-2 fad8 vte2-1, did not display the visual phenotype or the aberrant GST1 expression observed in vte2-1. Moreover, cotyledon bleaching in vte2-1 was chemically phenocopied by treatment of wild-type plants with MDA. These data suggest that products of tri-unsaturated fatty acid oxidation underlie the vte2-1 seedling phenotype, including cellular toxicity and gene regulation properties. Generation of the quadruple mutant facilitated the development of an in situ fluorescence assay based on the formation of adducts of MDA with 2-thiobarbituric acid at 37 °C. Specificity was verified by measuring pentafluorophenylhydrazine derivatives of MDA and by liquid chromatography analysis of MDA-2-thiobarbituric acid adducts. Potentially applicable to other organisms, this method allowed the localization of MDA pools throughout the body of Arabidopsis and revealed an undiscovered pool of the compound unlikely to be derived from trienoic fatty acids in the vicinity of the root tip quiescent center.

Received for publication, August 16, 2007 , and in revised form, October 9, 2007.

E. E. F. dedicates this work to the memory of his friend and mentor, Prof. C. A. "Bud" Ryan.

^* This work was supported by Swiss National Science Foundation Grant 3100A0-101711 and the Swiss National Science Foundation National Centre of Competence in Research Plant Survival Program. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Present address: Dept. of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824-1319.

² To whom correspondence should be addressed. Tel.: 41-21-692-4190; Fax: 41-21-692-4195; E-mail: edward.farmer{at}unil.ch.

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