Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis

Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis1,[W] Ilya Gadjev2, Sandy Vanderauwera2, Tsanko S. Gechev, Christophe Laloi, Ivan N. Minkov, Vladimir Shulaev, Klaus Apel, Dirk Inzé, Ron Mittler and Frank Van Breusegem* Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, B–9052 Gent, Belgium (I.G., S.V., D.I., F.V.B.); Department of Plant Physiology and Plant Molecular Biology, University of Plovdiv, Plovdiv 4000, Bulgaria (I.G., T.S.G., I.N.M.); Department Molecular Biology of Plants, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, NL–9751 NN Haren, The Netherlands (T.S.G.); Institute of Plant Sciences, Plant Genetics, Swiss Federal Institute of Technology, CH–8092 Zurich, Switzerland (C.L., K.A.); Department of Biochemistry, University of Nevada, Reno, Nevada 89557 (R.M.); and Virginia Bioinformatics Institute, Blacksburg, Virginia 24061 (V.S.) Reactive oxygen species (ROS) are key players in the regulation of plant development, stress responses, and programmed cell death. Previous studies indicated that depending on the type of ROS (hydrogen peroxide, superoxide, or singlet oxygen) or its subcellular production site (plastidic, cytosolic, peroxisomal, or apoplastic), a different physiological, biochemical, and molecular response is provoked. We used transcriptome data generated from ROS-related microarray experiments to assess the specificity of ROS-driven transcript expression. Data sets obtained by exogenous application of oxidative stress-causing agents (methyl viologen, Alternaria alternata toxin, 3-aminotriazole, and ozone) and from a mutant (fluorescent) and transgenic plants, in which the activity of an individual antioxidant enzyme was perturbed (catalase, cytosolic ascorbate peroxidase, and copper/zinc superoxide dismutase), were compared. In total, the abundance of nearly 26,000 transcripts of Arabidopsis (Arabidopsis thaliana) was monitored in response to different ROS. Overall, 8,056, 5,312, and 3,925 transcripts showed at least a 3-, 4-, or 5-fold change in expression, respectively. In addition to marker transcripts that were specifically regulated by hydrogen peroxide, superoxide, or singlet oxygen, several transcripts were identified as general oxidative stress response markers because their steady-state levels were at least 5-fold elevated in most experiments. We also assessed the expression characteristics of all annotated transcription factors and inferred new candidate regulatory transcripts that could be responsible for orchestrating the specific transcriptomic signatures triggered by different ROS. Our analysis provides a framework that will assist future efforts to address the impact of ROS signals within environmental stress conditions and elucidate the molecular mechanisms of the oxidative stress response in plants.