Shade triggers posttranscriptional Phytochrome- interacting factor-dependent increases in H3K4 trimethylation

Authors: CALDERON, R - University Of California Berkeley; DALTON, JUTTA - University Of California Berkeley; ZHANG, YU - University Of California Berkeley; QUAIL, PETER - University Of California Berkeley

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/16/2022
Publication Date: 6/8/2022
Citation: Calderon, R.H., Dalton, J., Zhang, Y., Quail, P.H. 2022. Shade triggers posttranscriptional Phytochrome- interacting factor-dependent increases in H3K4 trimethylation. Plant Physiology. Article kiac282. https://doi.org/10.1093/plphys/kiac282.
DOI: https://doi.org/10.1093/plphys/kiac282

Interpretive Summary: Plants use phytochrome (phy) photoreceptors, coupled directly to Phytochrome-Interacting transcription Factors (PIFs), as a phy-PIF sensory module, 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. Detection of such signals rapidly induces the changes in gene expression, that drive the adaptational growth and development appropriate to the environment. This study investigates the potential functional role of epigenetic chromatin modifications in mediating these rapid transcription-level responses to the shade signals. Time-resolved analysis shows that the shade-induced transcriptional increases precede such epigenetic changes, suggesting that chromatin remodeling is a consequence, rather than an initiator, of the changes in expression of shade-induced genes.

Technical Abstract: The phytochrome (phy)-PIF (Phytochrome Interacting Factor) sensory module perceives and transduces light signals to Direct-Target Genes (DTGs), which then drive the adaptational responses in plant growth and development, appropriate to the prevailing environment. These signals include the first exposure of etiolated seedlings to sunlight upon emergence from subterranean darkness, and the change in color of the light that is filtered through, or reflected from, neighboring vegetation (‘shade’). Previously, we identified three broad categories of rapidly signal-responsive genes: those repressed by light and conversely induced by shade; those repressed by light, but subsequently unresponsive to shade; and those responsive to shade only. Here, we investigate the potential role of epigenetic chromatin modifications in regulating these contrasting patterns of phy-PIF module-induced expression of DTGs. Using RNA-seq and ChIP-seq, time-resolved profiling of transcript and histone 3 lysine 4 trimethylation (H3K4me3) levels, respectively, we show that, whereas the initial dark-to-light transition triggers a rapid, apparently temporally-coincident decline of both parameters, the light-to-shade transition induces similarly rapid increases in transcript levels that precede increases in H3K4me3 levels. Together with other recent findings, these data raise the possibility that, rather than being causal in the shade-induced expression changes, H3K4me3 may function to buffer the rapidly fluctuating shade/light switching that is intrinsic to vegetational canopies under natural sunlight conditions.