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.In nature, plant growth is often limited by unfavourable conditions or disease. Plants have thus evolved sophisticated mechanisms to adapt to such stresses. In fact, brief exposure to stress can prime plants to be better prepared for a future stress following a period without stress. However, the molecular basis of this memory-like phenomenon is poorly understood.Now, Brzezinka, Altmann et al. have used priming by heat stress as a model to dissect the memory of environmental stresses in thale cress, Arabidopsis thaliana. First, a library of mutant plants were tested to identify a gene that is specifically required for heat stress memory but not for the initial responses to heat. Brzezinka, Altmann et al. identified one such gene and termed it FORGETTER1 (or FGT1 for short). Further experiments then revealed that the FGT1 protein binds directly to a specific class of heat-inducible genes that are relevant for heat stress memory.Brzezinka, Altmann et al. propose that the FGT1 protein makes sure that the heat-inducible genes are always accessible and active by modifying the way the DNA containing these genes is packaged. DNA is wrapped around protein complexes called nucleosomes and depending on how tightly the DNA of a gene is wrapped makes it more or less easy to activate the gene. In agreement with this model, FGT1 does interact with proteins that can reposition nucleosomes and leave the DNA more loosely packaged. Also, the fact that plants that lack a working FGT1 gene repackage the DNA of memory-related genes too early after experiencing heat stress provides further support for the model.Together these findings could lead to new approaches for breeding programmes to improve stress tolerance in crop plants. One future challenge will be to find out whether memories involving nucleosomes are also made in response to other stressful conditions, such as attack by pests and disease.