Soy, J., Leivar, P., González-Schain, N., Martín, G., Diaz, C., Sentandreu, M., Bassem Al-Sady, B., Quail, P. H., and Monte E. (2016). Molecular convergence of clock and photosensory pathways through PIF3-TOC1 interaction and co-occupancy of target promoters. Proc Natl Acad Sci USA 113: 4870-4875; 10.1073/pnas.1603745113
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-interacting factors). PIF protein abundance in SDs oscillates as a balance between synthesis and photoactivated-phytochrome-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 Timing of CAB expression 1 (TOC1) display coincident cobinding to the promoters of predawn-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 postdusk 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 postdusk, thereby gating growth to predawn, 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 phytochrome photosensory pathway to coregulate directly the activity of the PIF transcription factors positioned at the apex of a transcriptional network that regulates a diversity of downstream morphogenic responses.
Martın G, Leivar P,, Ludevid D , Tepperman JM, Quail PH & Monte E. (2016). Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network. Nature Communications 7:11431; 10.1038/ncomms114
Plastid-to-nucleus retrograde signals emitted by dysfunctional chloroplasts impact photomorphogenic development, but the molecular link between retrograde- and photosensory-receptor signalling has remained unclear. Here, we show that the phytochrome and retrograde signalling (RS) pathways converge antagonistically to regulate the expression of the nuclear-encoded transcription factor GLK1, a key regulator of a light-induced transcriptional network central to photomorphogenesis. GLK1 gene transcription is directly repressed by PHYTOCHROME-INTERACTING FACTOR (PIF)-class bHLH transcription factors in darkness, but light-activated phytochrome reverses this activity, thereby inducing expression. Conversely, we show that retrograde signals repress this induction by a mechanism independent of PIF mediation. Collectively, our data indicate that light at moderate levels acts through the plant’s nuclear-localized sensory-photoreceptor system to induce appropriate photomorphogenic development, but at excessive levels, sensed through the separate plastid-localized RS system, acts to suppress such development, thus providing a mechanism for protection against photo-oxidative damage by minimizing the tissue exposure to deleterious radiation.
Faculty1000 citation, by Christian Fankhauser, Univ. Lausanne
Basic helix-loop-helix (bHLH) transcription factors of the phytochrome interacting factor (PIF) family are important growth regulators affecting multiple aspects of plant growth and development. Their activity is carefully regulated at multiple levels including phytochrome-mediated control of protein stability. This interesting study shows that the circadian clock gates PIF3 activity through the activity of the circadian oscillator TOC1. TOC1 is a transcriptional repressor that binds to many PIF target genes. Rhythmic binding of TOC1 to these genes prevents PIF-mediated gene activation, thereby contributing to circadian regulation of PIF-controlled gene expression and growth promotion.