A stress-specific calcium signature regulating an ozone-responsive gene expression network in Arabidopsis

Changes in gene expression form a key component of the molecular mechanisms by which plants adapt and respond to environmental stresses. There is compelling evidence for the role of stimulus-specific Ca2+ signatures in plant stress responses. However, our understanding of how they orchestrate the differential expression of stress-induced genes remains fragmentary. We have undertaken a global study of changes in the Arabidopsis transcriptome induced by the pollutant ozone in order to establish a robust transcriptional response against which to test the ability of Ca2+ signatures to encode stimulus-specific transcriptional information. We show that the expression of a set of co-regulated ozone-induced genes is Ca2+-dependent and that abolition of the ozone-induced Ca2+ signature inhibits the induction of these genes by ozone. No induction of this set of ozone-regulated genes was observed in response to H2O2, one of the reactive oxygen species (ROS) generated by ozone, or cold stress, which also generates ROS, both of which stimulate changes in [Ca2+]cyt. These data establish unequivocally that the Ca2+-dependent changes in gene expression observed in response to ozone are not simply a consequence of an ROS-induced increase in [Ca2+]cytper se. The magnitude and temporal dynamics of the ozone, H2O2, and cold Ca2+ signatures all differ markedly. This finding is consistent with the hypothesis that stimulus-specific transcriptional information can be encoded in the spatiotemporal dynamics of complex Ca2+ signals in plants.