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Research Project: Dissecting the Mechanisms of Phytochrome Photoperception, Signaling and Gene Regulation

Location: Plant Gene Expression Center

Title: Chromatin changes in Phytochrome interacting factor-regulated genes parallel their rapid transcriptional response to light

item GONZALEZ-GRANDIO, EDUARDO - University Of California Berkeley
item ALAMOS, SIMON - University Of California Berkeley
item ZHANG, YU - University Of California Berkeley
item DALTON-ROESLER, JUTTA - University Of California Berkeley
item NIYOGI, KRISHNA - University Of California Berkeley
item GARCIA, HERNAN - University Of California Berkeley
item QUAIL, PETER - University Of California Berkeley

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/27/2021
Publication Date: 2/17/2022
Citation: Gonzalez-Grandio, E., Alamos, S., Zhang, Y., Dalton-Roesler, J., Niyogi, K.K., Garcia, H.G., Quail, P.H. 2022. Chromatin changes in Phytochrome interacting factor-regulated genes parallel their rapid transcriptional response to light. Frontiers in Plant Science. 13. Article 803441.

Interpretive Summary: It is well-established that light-activated phytochrome (phy) photoreceptor molecules induce rapid gene expression changes via direct binding to promoter-bound PIF transcription factors, upon initial emergence of germinating seedlings from subterranean darkness. This paper investigated the potential role of chromatin remodeling as an intermediary in the light-triggered regulation of PIF-Direct Target Genes (DTGs). Time-resolved analysis shows that the levels of the chromatin mark, H3K9ac, change, within minutes of initial light exposure, in parallel with the light-induced transcriptional changes in the corresponding DTGs. The data suggest, therefore, that chromatin remodeling is mechanistically, integrally involved in the very initial light-responsive transcriptional changes of these genes.

Technical Abstract: As sessile organisms, plants must adapt to a changing environment, sensing variations in resource availability and modifying their development in response. Light is one of the most important resources for plants, and its perception by sensory photoreceptors (e.g., phytochromes) and subsequent transduction into long-term transcriptional reprogramming have been well characterized. Chromatin changes have been shown to be involved in photomorphogenesis. However, the initial short-term transcriptional changes produced by light and what factors enable these rapid changes are not well studied. Here, we define rapidly light-responsive, Phytochrome Interacting Factor (PIF)direct-target genes (LRP-DTGs). We found that a majority of these genes also show rapid changes in Histone 3 Lysine-9 acetylation (H3K9ac) in response to the light signal. Detailed time-course analysis of transcript and chromatin changes showed that,for light-repressed genes, H3K9 deacetylation parallels light-triggered transcriptional repression, while for light-induced genes, H3K9 acetylation appeared to somewhat precede light-activated transcript accumulation. However, direct, real-time imaging of transcript elongation in the nucleus revealed that, in fact, transcriptional induction actually parallels H3K9 acetylation. Collectively, the data raise the possibility that light-induced transcriptional and chromatin-remodeling processes are mechanistically intertwined. Histone modifying proteins involved in long term light responses do not seem to have a role in this fast response, indicating that different factors might act at different stages of the light response. This work not only advances our understanding of plant responses to light, but also unveils a system in which rapid chromatin changes in reaction to an external signal can be studied under natural conditions.