phyA dominates in transduction of red-light signals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation

Contrary to expectations based on the visible phenotypic behavior of seedlings undergoing de-etiolation in response to continuous red light (Rc), previous gene expression profiling showed that one or more of the five-membered phytochrome (phy) family of Arabidopsis, other than phyB, is predominantly responsible for transducing the Rc signals to light-responsive genes. To begin to identify which phys are involved, and to define potential primary targets of phy signaling, we have examined the genome-wide expression profiles of genes responding to Rc within 1 h (early response genes) of initial exposure of dark-grown wild-type, phyA, phyB and phyAphyB double mutant seedlings to the light signal. The data show that phyA has a quantitatively dominant role in Rc-induced expression of these early response genes, that phyB has minimal detectable regulatory activity in the presence of phyA, but assumes a quantitatively larger role in its absence, and that phyA and phyB combined are responsible for the full extent of Rc responsiveness of 96% of these genes. No evidence was obtained of a significant role for the remaining family members, phyC, phyD or phyE, in this process. In striking contrast, Rc-imposed repression of early response gene expression remains quantitatively strong in the phyAphyB double mutant, as well as the monogenic mutants, suggesting a significant role for one or more of the other three phys in this response. Examination of the established or predicted functional roles of the early response genes indicates that genes encoding transcription factors represent the largest single category, at a frequency three times their prevalence genome-wide. This dominance is particularly striking among those genes responding most robustly to the Rc signal, where >50% are classified as involved in transcriptional regulation, suggesting that these may have potentially primary regulatory roles at the interface between phy signaling and the light-responsive transcriptional network. Integration of the present data with those of a previous genome-scale transcriptional analysis of a pif3 mutant, suggests a complex network involving perception and transduction of inductive Rc signals by both phyA and phyB through both PIF3 and other undefined signaling partners to early response genes.