Central clock components modulate plant shade avoidance by directly repressing transcriptional activation activity of PIF proteins

Authors: ZHANG, YU - University Of California; PFEIFFER, ANN - University Of California; TEPPERMAN, JAMES - University Of California; DALTON-ROESLER, JUTTA - University Of California; LEIVAR, PABLO - University Of California; GRANDIO, EDUARDO - University Of California; Quail, Peter

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/27/2020
Publication Date: 2/11/2020
Citation: Zhang, Y., Pfeiffer, A., Tepperman, J.M., Dalton-Roesler, J., Leivar, P., Quail, P. 2020. Central clock components modulate plant shade avoidance by directly repressing transcriptional activation activity of PIF proteins. Proceedings of the National Academy of Sciences. 117(6):3261-3269. https://doi.org/10.1073/pnas.1918317117.
DOI: https://doi.org/10.1073/pnas.1918317117

Interpretive Summary: Plants use phytochrome photoreceptors to monitor for the presence of competitors for photosynthetically active sunlight. They do so by sensing near-proximity or direct shade (“shade signals”) from neighboring vegetation. This study defines the functional role, and molecular mechanism of action, of Pseudo-Response Regulator proteins (PRRs) (integral components of the plant central circadian oscillator) in regulating growth responses to such signals. These PRRs are shown to bind, intranuclearly, directly to members of the Phytochrome Interacting Factor (PIF) family of transcription factors, repressing their capacity to transcriptionally activate a subset of their Direct Target Genes. These findings show that the plant clock communicates with the genome using direct, physical interaction of multiple central oscillator components with the transcriptional-regulatory machinery of the cell.

Technical Abstract: Light-environment signals, sensed by plant phytochrome photoreceptors, are transduced to target genes through direct regulation of PHYTOCHROME-INTERACTING FACTOR (PIF) transcription factor abundance and activity. Previous genome-wide DNA-binding and expression analysis has identified a set of genes that are direct targets of PIF transcriptional regulation. However, quantitative analysis of promoter occupancy versus expression level has suggested that unknown "trans factors" modulate the intrinsic transcriptional activation activity of DNA-bound PIF proteins. Here, using computational analysis of published data, we have identified PSEUDO-RESPONSE REGULATORS (PRR5 and PRR7) as displaying a high frequency of colocalization with the PIF proteins at their binding sites in the promoters of PIF Direct Target Genes (DTGs). We show that the PRRs function to suppress PIF-stimulated growth in the light and vegetative shade and that they repress the rapid PIF-induced expression of PIF-DTGs triggered by exposure to shade. The repressive action of the PRRs on both growth and DTG expression requires the PIFs, indicating direct action on PIF activity, rather than a parallel antagonistic pathway. Protein interaction assays indicate that the PRRs exert their repressive activity by binding directly to the PIF proteins in the nucleus. These findings support the conclusion that the PRRs function as direct outputs from the core circadian oscillator to regulate the expression of PIF-DTGs through modulation of PIF transcriptional activation activity, thus expanding the roles of the multifunctional PIF-signaling hub.