Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling

Abstract

Plants as sessile organisms can adapt to environmental stress to mitigate its adverse effects. As part of such adaptation they maintain an active memory of heat stress for several days that promotes a more efficient response to recurring stress. We show that this heat stress memory requires the activity of the FORGETTER1 (FGT1) locus, with fgt1 mutants displaying reduced maintenance of heat-induced gene expression. FGT1 encodes the Arabidopsis thaliana orthologue of Strawberry notch (Sno), and the protein globally associates with the promoter regions of actively expressed genes in a heat-dependent fashion. FGT1 interacts with chromatin remodelers of the SWI/SNF and ISWI families, which also display reduced heat stress memory. Genomic targets of the BRM remodeler overlap significantly with FGT1 targets. Accordingly, nucleosome dynamics at loci with altered maintenance of heat-induced expression are affected in fgt1. Together, our results suggest that by modulating nucleosome occupancy, FGT1 mediates stress-induced chromatin memory.DOI: http://dx.doi.org/10.7554/eLife.17061.001

The histone variant H2A.Z and chromatin remodeler BRAHMA act coordinately and antagonistically to regulate transcription and nucleosome dynamics in Arabidopsis

“…BRM and H2A.Z have been associated with +1 nucleosome stability in combination with other factors as well. Mutants for the FORGETTER1 TF that interacts with BRM perturb +1 nucleosome occupancy of genes involved in heat stress memory (Brzezinka et al ., ). Our data showing an increase in +1 nucleosome occupancy in brm mutants support a role for BRM in contributing to how FORGETTER1 destabilizes +1 nucleosomes after heat exposure.…”

Distinct heat shock factors and chromatin modifications mediate the organ‐autonomous transcriptional memory of heat stress

“…Heat stress activates transcriptional memory, as evident from both sustained activation of gene expression after HS and stronger reactivation of gene expression upon a recurring HS. This transcriptional memory is associated with elevated histone H3K4 methylation and enhanced gene accessibility (Brzezinka et al ., ; Lämke et al ., ); however, in‐depth characterization and mechanistic understanding are still incomplete. Here, we have reported a detailed characterization of the enhanced re‐induction transcriptional memory with respect to its genome‐wide extent, kinetics and mechanism.…”

“…Mutant and complementation lines of hsfa2, the hsfa1a hsfa1b hsfa1d triple mutant and the transgenic line with HSFA2 constitutively overexpressed in HSFA1 quadruple mutant were previously described (Charng et al, 2007;Liu et al, 2011;Liu and Charng, 2013). Growth conditions on Murashige and Skoog medium at 22°C were as previously described (Liu et al, 2011;Brzezinka et al, 2016). The priming HS was performed at 4 days after germination for gene expression and chromatin immunoprecipitation (ChIP) experiments.…”

“…Priming is generally defined as a phenomenon in which a transient biotic or abiotic stress cue leads to modified (typically faster or stronger) defense responses upon exposure to a recurring stress (Conrath, 2011;Hilker et al, 2015;L€ amke and B€ aurle, 2017). Heat stress memory is the active maintenance of acquired thermotolerance and is genetically separable from it, as evidenced by mutants that acquire thermotolerance normally but are unable to maintain it (Charng et al, 2006(Charng et al, , 2007Stief et al, 2014;Brzezinka et al, 2016). However, the molecular basis of HS memory is not understood.…”

Remembrance of stresses past: heat shock factors and histone hypermethylation are key

“…Plants that are stressed can cope with a subsequent stress a bit better, a process termed priming (Lämke and Bäurle, ). The ability to acquire tolerance to a stress is separable from the ability to retain memory of a stress, as deduced by studying mutants such as FORGETTER1 (Brzezinka et al ., ). The heat shock response has several components: heat shock transcription factors (HSFs) that are activated upon a heat shock and are thought to be master regulators, as they subsequently induce transcription of numerous target genes, including those encoding heat shock proteins.…”