Plant Cell Advance Online Publication
Published on December 17, 2004; 10.1105/tpc.104.026971
Received August 16, 2004
Accepted November 10, 2004
Cytosolic Ascorbate Peroxidase 1 Is a Central Component of the Reactive Oxygen Gene Network of Arabidopsis
Sholpan Davletova 1, Ludmila Rizhsky 2, Hongjian Liang 2, Zhong Shengqiang 2, David J. Oliver 2, Jesse Coutu 1, Vladimir Shulaev 3, Karen Schlauch 4, and Ron Mittler 1*
1 Department of Biochemistry and Molecular Biology, University of Nevada, Reno, Nevada 89557
2 Department of Genetics and Developmental and Cell Biology, Iowa State University, Ames, Iowa 50011
3 Virginia Bioinformatics Institute, Blacksburg, Virginia 24061
4 Center for Biomedical Genomics and Informatics, George Mason University, Manassas, Virginia 20110
* To whom correspondence should be addressed. E-mail: ronm{at}unr.edu.
Reactive oxygen species (ROS), such as O2- and H2O2, play a key role in plant metabolism, cellular signaling, and defense. In leaf cells, the chloroplast is considered to be a focal point of ROS metabolism. It is a major producer of O2- and H2O2 during photosynthesis, and it contains a large array of ROS-scavenging mechanisms that have been extensively studied. By contrast, the function of the cytosolic ROS-scavenging mechanisms of leaf cells is largely unknown. In this study, we demonstrate that in the absence of the cytosolic H2O2-scavenging enzyme ascorbate peroxidase 1 (APX1), the entire chloroplastic H2O2-scavenging system of Arabidopsis thaliana collapses, H2O2 levels increase, and protein oxidation occurs. We further identify specific proteins oxidized in APX1-deficient plants and characterize the signaling events that ensue in knockout-Apx1 plants in response to a moderate level of light stress. Using a dominant-negative approach, we demonstrate that heat shock transcription factors play a central role in the early sensing of H2O2 stress in plants. Using knockout plants for the NADPH oxidase D protein (knockout-RbohD), we demonstrate that RbohD might be required for ROS signal amplification during light stress. Our study points to a key role for the cytosol in protecting the chloroplast during light stress and provides evidence for cross-compartment protection of thylakoid and stromal/mitochondrial APXs by cytosolic APX1.
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