In plants, epidermal guard cells integrate and respond to numerous environmental signals to control stomatal pore apertures, thereby regulating gas exchange. Chromatin structure controls transcription factor (TF) access to the genome, but whether large-scale chromatin remodeling occurs in guard cells during stomatal movements, and in response to the hormone abscisic acid (ABA) in general, remains unknown. Here, we isolate guard cell nuclei fromArabidopsis thalianaplants to examine whether the physiological signals, ABA and CO2(carbon dioxide), regulate guard cell chromatin during stomatal movements. Our cell type–specific analyses uncover patterns of chromatin accessibility specific to guard cells and define cis-regulatory sequences supporting guard cell–specific gene expression. We find that ABA triggers extensive and dynamic chromatin remodeling in guard cells, roots, and mesophyll cells with clear patterns of cell type specificity. DNA motif analyses uncover binding sites for distinct TFs enriched in ABA-induced and ABA-repressed chromatin. We identify the Abscisic Acid Response Element (ABRE) Binding Factor (ABF) bZIP-type TFs that are required for ABA-triggered chromatin opening in guard cells and roots and implicate the inhibition of a clade of bHLH-type TFs in controlling ABA-repressed chromatin. Moreover, we demonstrate that ABA and CO2induce distinct programs of chromatin remodeling, whereby elevated atmospheric CO2had only minimal impact on chromatin dynamics. We provide insight into the control of guard cell chromatin dynamics and propose that ABA-induced chromatin remodeling primes the genome for abiotic stress resistance.
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Warming triggers stomatal opening by enhancement of photosynthesis and ensuing guard cell CO2 sensing, whereas higher temperatures induce a photosynthesis‐uncoupled response
Summary Plants integrate environmental stimuli to optimize photosynthesis vs water loss by controlling stomatal apertures. However, stomatal responses to temperature elevation and the underlying molecular genetic mechanisms remain less studied.We developed an approach for clamping leaf‐to‐air vapor pressure difference (VPDleaf) to fixed values, and recorded robust reversible warming‐induced stomatal opening in intact plants. We analyzed stomatal temperature responses of mutants impaired in guard cell signaling pathways for blue light, abscisic acid (ABA), CO2, and the temperature‐sensitive proteins, Phytochrome B (phyB) and EARLY‐FLOWERING‐3 (ELF3).We confirmed thatphot1‐5/phot2‐1leaves lacking blue‐light photoreceptors showed partially reduced warming‐induced stomatal opening. Furthermore, ABA‐biosynthesis, phyB, and ELF3 were not essential for the stomatal warming response. Strikingly,Arabidopsis(dicot) andBrachypodium distachyon(monocot) mutants lacking guard cell CO2sensors and signaling mechanisms, includinght1,mpk12/mpk4‐gc, andcbc1/cbc2abolished the stomatal warming response, suggesting a conserved mechanism across diverse plant lineages. Moreover, warming rapidly stimulated photosynthesis, resulting in a reduction in intercellular (CO2). Interestingly, further enhancing heat stress caused stomatal opening uncoupled from photosynthesis.We provide genetic and physiological evidence that the stomatal warming response is triggered by increased CO2assimilation and stomatal CO2sensing. Additionally, increasing heat stress functions via a distinct photosynthesis‐uncoupled stomatal opening pathway.
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- PAR ID:
- 10583777
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 244
- Issue:
- 5
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- 1847 to 1863
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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