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Abstract Environmental stimuli trigger rapid transcriptional reprogramming of gene networks. These responses occur in the context of the local chromatin landscape, but the contribution of organ-specific dynamic chromatin modifications in responses to external signals remains largely unexplored. We treated tomato seedlings with a supply of nitrate and measured the genome-wide changes of four histone marks, the permissive marks H3K27ac, H3K4me3, and H3K36me3 and repressive mark H3K27me3, in shoots and roots separately, as well as H3K9me2 in shoots. Dynamic and organ-specific histone acetylation and methylation were observed at functionally relevant gene loci. Integration of transcriptomic and epigenomic datasets generated from the same organ revealed largely syngenetic relations between changes in transcript levels and histone modifications, with the exception of H3K27me3 in shoots, where an increased level of this repressive mark is observed at genes activated by nitrate. Application of a machine learning approach revealed organ-specific rules regarding the importance of individual histone marks, as H3K36me3 is the most successful mark in predicting gene regulation events in shoots, while H3K4me3 is the strongest individual predictor in roots. Our integrated study substantiates a view that during plant environmental responses, the relationships between histone code dynamics and gene regulation are highly dependent on organ-specific contexts.
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Chromatin Changes in Phytochrome Interacting Factor-Regulated Genes Parallel Their Rapid Transcriptional Response to Light
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.
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- Award ID(s):
- 1652236
- PAR ID:
- 10382188
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 13
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Light serves as a pivotal environmental cue regulating various aspects of plant growth and development, including seed germination, seedling de-etiolation, and shade avoidance. Within this regulatory framework, the basic helix–loop–helix transcription factors known as phytochrome-interacting factors (PIFs) play an essential role in orchestrating responses to light stimuli. Phytochromes, acting as red/far-red light receptors, initiate a cascade of events leading to the degradation of PIFs (except PIF7), thereby triggering transcriptional reprogramming to facilitate photomorphogenesis. Recent research has unveiled multiple post-translational modifications that regulate the abundance and/or activity of PIFs, including phosphorylation, dephosphorylation, ubiquitination, deubiquitination, and SUMOylation. Moreover, intriguing findings indicate that PIFs can influence chromatin modifications. These include modulation of histone 3 lysine 9 acetylation (H3K9ac), as well as occupancy of histone variants such as H2A.Z (associated with gene repression) and H3.3 (associated with gene activation), thereby intricately regulating downstream gene expression in response to environmental cues. This review summarizes recent advances in understanding the role of PIFs in regulating various signaling pathways, with a major focus on photomorphogenesis.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2022.803441
