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First published online June 7, 2007; 10.1104/pp.107.101436

Plant Physiology 144:1777-1785 (2007)
© 2007 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Double Mutants Deficient in Cytosolic and Thylakoid Ascorbate Peroxidase Reveal a Complex Mode of Interaction between Reactive Oxygen Species, Plant Development, and Response to Abiotic Stresses1,[W],[OA]

Gad Miller, Nobuhiro Suzuki, Ludmila Rizhsky, Alicia Hegie, Shai Koussevitzky and Ron Mittler*

Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada 89557 (G.M., N.S., A.H., S.K., R.M.); Department of Genetics, Development and Cell Biology, Iowa State University, Ames, Iowa 50011 (L.R.); and Department of Plant Sciences, Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel (R.M.)

Reactive oxygen species (ROS) play a key signaling role in plants and are controlled in cells by a complex network of ROS metabolizing enzymes found in several different cellular compartments. To study how different ROS signals, generated in different cellular compartments, are integrated in cells, we generated a double mutant lacking thylakoid ascorbate peroxidase (tylapx) and cytosolic ascorbate peroxidase1 (apx1). Our analysis suggests that two different signals are generated in plants lacking cytosolic APX1 or tylAPX. The lack of a chloroplastic hydrogen peroxide removal enzyme triggers a specific signal in cells that results in enhanced tolerance to heat stress, whereas the lack of a cytosolic hydrogen peroxide removal enzyme triggers a different signal, which results in stunted growth and enhanced sensitivity to oxidative stress. When the two signals are coactivated in cells (i.e. tylapx/apx1), a new response is detected, suggesting that the integration of the two different signals results in a new signal that manifests in late flowering, low protein oxidation during light stress, and enhanced accumulation of anthocyanins. Our results demonstrate a high degree of plasticity in ROS signaling in Arabidopsis (Arabidopsis thaliana) and suggest the existence of redundant pathways for ROS protection that compensate for the lack of classical ROS removal enzymes such as cytosolic and chloroplastic APXs. Further investigation of the enhanced heat tolerance in plants lacking tylAPX, using mutants deficient in chloroplast-to-nuclei retrograde signaling, suggests the existence of a chloroplast-generated stress signal that enhances basal thermotolerance in plants.


1 This work was supported by the National Science Foundation (grant nos. IBN–0420033 and NSF–0431327), by the Nevada Agricultural Experimental Station, and by the National Institutes of Health IDeA Network of Biomedical Research Excellence (grant no. INBRE P20 RR 016464–05).

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: Ron Mittler (ronm{at}unr.edu).

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

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.101436

* Corresponding author; e-mail ronm{at}unr.edu; fax 775–784–1650.

Received April 23, 2007; accepted May 21, 2007; published June 7, 2007.




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