Many environmental conditions fluctuate and organisms need to respond effectively. This is especially true for temperature cues that can change in minutes to seasons and often follow a diurnal rhythm. Plants cannot migrate and most cannot regulate their temperature. Therefore, a broad array of responses evolved to deal with temperature cues from freezing to heat stress. A particular response to mildly elevated temperatures is called thermomorphogenesis, a suite of morphological adaptations that includes thermonasty, formation of thin leaves and elongation growth of petioles and hypocotyl. Thermomorphogenesis allows for optimal performance in suboptimal temperature conditions by enhancing cooling capacity. When temperatures rise further, heat stress tolerance mechanisms can be induced that enable the plant to survive the stressful temperature, which typically comprises of cellular protection mechanisms and memory thereof. Induction of thermomorphogenesis, heat stress tolerance and stress memory depend on gene expression regulation, governed by diverse epigenetic processes. In this Tansley review we update on the current knowledge of epigenetic regulation of heat stress tolerance and elevated temperature signalling and response, with a focus on thermomorphogenesis regulation and heat stress memory. In particular we highlight the emerging role of H3K4 methylation marks in diverse temperature signalling pathways.

Epigenetic regulation of thermomorphogenesis and heat stress tolerance.

Abstract The size of plant organs is highly responsive to environmental conditions. The plant’s embryonic stem, or hypocotyl, displays phenotypic plasticity, in response to light and temperature. The hypocotyl of shade avoiding species elongates to outcompete neighboring plants and secure access to sunlight. Similar elongation occurs in high temperature. However, it is poorly understood how environmental light and temperature cues interact to effect plant growth. We found that shade combined with warm temperature produces a synergistic hypocotyl growth response that dependent on PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) and auxin. This unique but agriculturally relevant scenario was almost totally independent on PIF4 activity. We show that warm temperature is sufficient to promote PIF7 DNA binding but not transcriptional activation and we demonstrate that additional, unknown factor/s must be working downstream of the phyB-PIF-auxin module. Our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density. 

/pdf/pif7-is-a-master-regulator-of-thermomorphogenesis-in-shade-3968jw8o.pdf

PIF7 is a master regulator of thermomorphogenesis in shade

Global warming impacts crop production and threatens food security. Elevated temperatures are sensed by different cell components. Temperature increases are classified as either mild warm temperatures or excessively hot temperatures, which are perceived by distinct signaling pathways in plants. Warm temperatures induce thermomorphogenesis, while high-temperature stress triggers heat acclimation and has destructive effects on plant growth and development. In this review, we systematically summarize the heat-responsive genetic networks in Arabidopsis and crop plants based on recent studies. In addition, we highlight the strategies used to improve grain yield under heat stress from a source-sink perspective. We also discuss the remaining issues regarding the characteristics of thermosensors and the urgency required to explore the basis of acclimation under multifactorial stress combination. 

The molecular basis of heat stress responses in plants.

/pdf/deep-inside-the-epigenetic-memories-of-stressed-plants-3bhubr7k.pdf

Deep inside the epigenetic memories of stressed plants.

Abstract Nucleosomal acetyltransferase of H4 (NuA4) is an essential transcriptional coactivator in eukaryotes, but remains poorly characterized in plants. Here, we describe Arabidopsis homologs of the NuA4 scaffold proteins Enhancer of Polycomb-Like 1 (AtEPL1) and Esa1-Associated Factor 1 (AtEAF1). Loss of AtEAF1 results in inhibition of growth and chloroplast development. These effects are stronger in the Atepl1 mutant and are further enhanced by loss of Golden2-Like (GLK) transcription factors, suggesting that NuA4 activates nuclear plastid genes alongside GLK. We demonstrate that AtEPL1 is necessary for nucleosomal acetylation of histones H4 and H2A.Z by NuA4 in vitro. These chromatin marks are diminished genome-wide in Atepl1 , while another active chromatin mark, H3K9 acetylation (H3K9ac), is locally enhanced. Expression of many chloroplast-related genes depends on NuA4, as they are downregulated with loss of H4ac and H2A.Zac. Finally, we demonstrate that NuA4 promotes H2A.Z deposition and by doing so prevents spurious activation of stress response genes. 

/pdf/nua4-and-h2a-z-control-environmental-responses-and-2ln3zj2a.pdf

NuA4 and H2A.Z control environmental responses and autotrophic growth in Arabidopsis

The interplay between light receptors and PHYTOCHROME-INTERACTING FACTORs (PIFs) serves as a regulatory hub that perceives and integrates environmental cues into transcriptional networks of plants1,2. Although occupancy of the histone variant H2A.Z and acetylation of histone H3 have emerged as regulators of environmentally responsive gene networks, how these epigenomic features interface with PIF activity is poorly understood3-7. By taking advantage of rapid and reversible light-mediated manipulation of PIF7 subnuclear localization and phosphorylation, we simultaneously assayed the DNA-binding properties of PIF7, as well as its impact on chromatin dynamics genome wide. We found that PIFs act rapidly to reshape the H2A.Z and H3K9ac epigenetic landscape in response to a change in light quality. Furthermore, we discovered that PIFs achieve H2A.Z removal through direct interaction with EIN6 ENHANCER (EEN), the Arabidopsis thaliana homolog of the chromatin remodeling complex subunit INO80 Subunit 6 (Ies6). Thus, we describe a PIF-INO80 regulatory module that is an intermediate step for allowing plants to change their growth trajectory in response to environmental changes.

PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants.

Author Correction: PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants

The pivotal interplay between light receptors and PHYTOCHROME INTERACTING FACTORs (PIFs) serves as an essential regulatory hub that perceives and integrates environmental cues into the plant’s transcriptional networks. A critical control component of environmentally-responsive gene networks is the histone variant H2A.Z which provides transcriptional plasticity and prevents undesired gene activation. However, the functional relationship between PIF transcription factors and H2A.Z is only poorly understood. Here, we describe a genomic approach that utilizes the rapid and reversible light-mediated manipulation of PIF7 activity to visualize PIF7 DNA binding and H2A.Z occupancy kinetics. Strikingly, PIFs shape the H2A.Z landscape in a light quality-dependent manner. In addition, we observed that PIFs initiate H2A.Z eviction through direct interaction with EIN6 ENHANCER (EEN), a subunit of INO80 chromatin remodeling complex. These studies uncover a previously unknown PIF-INO80 regulatory module controlling plant growth in response to rapid environmental changes. One-sentence summary A PIF-INO80 module controls light quality-dependent H2A.Z dynamics.

https://www.biorxiv.org/content/biorxiv/early/2019/11/01/826842.full.pdf

PHYTOCHROME INTERACTING FACTORs trigger environmentally responsive chromatin dynamics

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PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants.

Author Correction: PHYTOCHROME-INTERACTING FACTORs trigger environmentally responsive chromatin dynamics in plants

PHYTOCHROME INTERACTING FACTORs trigger environmentally responsive chromatin dynamics