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Title: Molecular convergence of cloc and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target populations

Author
item SOY, J - University Of California
item LEIVAR, P - University Of California
item GONZALEZ-SCHAIN, N - University Of California
item MARTIN, G - University Of California
item DIAZ, C - University Of California
item SENTANDREA, M - University Of California
item BASSEM AL SADY, B - University Of California
item QUAIL, P.H. - University Of California
item MONTE, E - University Of California

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/2/2014
Publication Date: 10/21/2014
Citation: Soy, J., Leivar, P., Gonzalez-Schain, N., Martin, G., Diaz, C., Sentandrea, M., Bassem Al Sady, B., Quail, P., Monte, E. 2014. Molecular convergence of cloc and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target populations. Proceedings of the National Academy of Sciences. 113(17):4870-4875.

Interpretive Summary: This study defines a molecular mechanism for how clock- and light-signaling pathways converge in Arabidopsis. The data reveal that TOC1, an essential core component of the central oscillator, binds to and represses PIF transcriptional activators, which are also the direct molecular signaling partners of the phytochrome photosensory receptors. This finding shows that TOC1 functions as a clock output-transducer, directly linking the core oscillator to a pleiotopically-acting transcriptional network, through repression of target genes. Collectively, in the plant, these components comprise a transcriptionally-centered signaling hub that provides clock-imposed gating of PIF-mediated, photosensory-regulated diurnal growth patterns. These results provide a framework for future research aimed at understanding how circadian dynamics are integrated with other plant physiological processes important for optimal plant fitness.

Technical Abstract: A mechanism for integrating light perception and the endogenous circadian clock is central to a plant’s capacity to coordinate its growth and development with the prevailing daily light/dark cycles. Under short-day (SD) photocycles, hypocotyl elongation is maximal at dawn, being promoted by the collective activity of a quartet of transcription factors, called PIF1, PIF3, PIF4, and PIF5 (Phytochrome (phy)-Interacting Factors). PIF protein abundance in SDs oscillates as a balance between synthesis and photoactivated-phy-imposed degradation, with maximum levels accumulating at the end of the long night. Previous evidence shows that elongation under diurnal conditions (as well as in shade) is also subjected to circadian gating. However, the mechanism underlying these phenomena is incompletely understood. Here, we show that the PIFs and the core-clock component, TOC1, display coincident co-binding to the promoters of pre-dawn-phased, growth-related genes under SD conditions. TOC1 interacts with the PIFs and represses their transcriptional activation activity, antagonizing PIF-induced growth. Given the dynamics of TOC1 abundance (displaying high post-dusk levels that progressively decline during the long night), our data suggest that TOC1 functions to provide a direct output from the core clock that transiently constrains the growth-promoting activity of the accumulating PIFs, early post-dusk, thereby gating growth to pre-dawn, when conditions for cell elongation are optimal. These findings unveil a previously-unrecognized mechanism whereby a core-circadian-clock output-signal converges immediately with the phy-photosensory pathway to directly co-regulate the activity of the PIF transcription factors, positioned at the apex of a transcriptional network that regulates a diversity of downstream morphogenic responses.