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J. Biol. Chem., Vol. 283, Issue 49, 34197-34203, December 5, 2008

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Ascorbate Peroxidase 1 Plays a Key Role in the Response of Arabidopsis thaliana to Stress Combination^*

Shai Koussevitzky, Nobuhiro Suzuki, Serena Huntington, Leigh Armijo, Wei Sha, Diego Cortes, Vladimir Shulaev, and Ron Mittler^¶1

From the Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada 89557, the Virginia Bioinformatics Institute, Blacksburg, Virginia 24061, and the ^¶Department of Plant Sciences, Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel

Within their natural habitat plants are subjected to a combination of different abiotic stresses, each with the potential to exacerbate the damage caused by the others. One of the most devastating stress combinations for crop productivity, which frequently occurs in the field, is drought and heat stress. In this study we conducted proteomic and metabolic analysis of Arabidopsis thaliana plants subjected to a combination of drought and heat stress. We identified 45 different proteins that specifically accumulated in Arabidopsis in response to the stress combination. These included enzymes involved in reactive oxygen detoxification, malate metabolism, and the Calvin cycle. The accumulation of malic enzyme during the combined stress corresponded with enhanced malic enzyme activity, a decrease in malic acid, and lower amounts of oxaloacetate, suggesting that malate metabolism plays an important role in the response of Arabidopsis to the stress combination. Cytosolic ascorbate peroxidase 1 (APX1) protein and mRNA accumulated during the stress combination. When exposed to heat stress combined with drought, an APX1-deficient mutant (apx1) accumulated more hydrogen peroxide and was significantly more sensitive to the stress combination than wild type. In contrast, mutants deficient in thylakoid or stromal/mitochondrial APXs were not more sensitive to the stress combination than apx1 or wild type. Our findings suggest that cytosolic APX1 plays a key role in the acclimation of plants to a combination of drought and heat stress.

Received for publication, August 15, 2008 , and in revised form, September 24, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grants RR-03-008 and P20 RR16464-05 from the IDeA Network of Biomedical Research Excellence. This work was also supported by National Science Foundation Grants IBN-0420033, NSF-0431327, and IOS-0743954 and The Nevada Agricultural Experimental Station (Publication 03055517). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental text, references, Tables S1 and S3, and Figs. S1–S5.

¹ To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, University of Nevada, Mail Stop 200, Reno, NV 89557. Tel.: 775-784-1384; Fax: 775-784-1650; E-mail: ronm{at}unr.edu.

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