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Published on June 7, 2007; 10.1104/pp.107.101436

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Received April 23, 2007
Accepted May 21, 2007

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 Stresses

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

Department of Biochemistry and Molecular Biology, University of Nevada, Mail Stop 200, Reno NV 89557; Department of Genetics, Development and Cell Biology, Iowa State University, Room 353 Bessey Hall, Ames, Iowa 50011; Department of Plant Sciences, Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel

* Corresponding author; email: ronm{at}unr.edu.

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 peroxidase 1 (apx1). Our analysis suggests that two different signals are generated in plants lacking cytosolic APX1 or tylAPX. The lack of a chloroplastic H2O2-removal enzyme triggers a specific signal in cells that results in enhanced tolerance to heat stress, whereas the lack of a cytosolic H2O2-removal enzyme triggers a different signal that results in stunted growth and enhanced sensitivity to oxidative stress. When the two signals are co-activated 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 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 mutant deficient in chloroplast-to-nuclei retrograde signaling, suggest the existence of a chloroplast-generated stress signal that enhances basal thermotolerance in plants.




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