ARC CoE Plant Energy Biology, University of Western Australia, 35 Stirling Highway, 6009 Crawley, WA.
Throughout the life of a plant, biogenesis and fine-tuning of energy organelles is essential both under normal growth and stress conditions. Communication from organelle to nucleus is thus essential to adapt gene regulation and protein synthesis specifically to the current needs of the plant. This organelle-to-nuclear communication is termed retrograde signaling and has been studied extensively over the last decades. Using large-scale gene expression data sets relating to perturbations of chloroplast and mitochondrial function, we have shown a highly significant overlap between gene expression changes triggered by chloroplast and mitochondrial perturbations. These overlapping gene expression changes appear to be common with general abiotic, biotic, and nutrient stresses. However, retrograde signaling pathways are also capable of distinguishing the source of the perturbation and subsets of genes are only responding to malfunction of each specific organelle. Our analysis suggested that WRKY transcription factors play a coordinating role on the interface of both organellar signaling pathways. Therefore we screened the 72 annotated WRKY transcription factors of Arabidopsis thaliana for binding to the promoters of genes responding to organellar dysfunction. Transgenic overexpression and knockout lines for multiple binding WRKY factors were generated and tested for altered expression of the marker genes during normal and stress conditions. This analysis demonstrated that AtWRKY40 and AtWRKY63 are particularly involved in regulating the expression of genes responding commonly to both mitochondrial and chloroplast dysfunction, but not of genes responding to either mitochondrial or chloroplast perturbation. In conclusion, this study establishes the role of WRKY transcription factors in the coordination of mitochondrial and chloroplast function during environmental stress conditions.