Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis

Aleksandra Skirycz,Vicky Oberkofler,Thomas Friedrich,Alexander Graf,Ewelina Sokolowska,Isabel Bäurle,Michal Gorka,Jörn Lämke,Krzysztof Brzezinka,Inês Trindade,Christian Kappel,Simone Altmann

doi:10.1038/s41467-021-23786-6

Abstract

Adaptive plasticity in stress responses is a key element of plant survival strategies. For instance, moderate heat stress (HS) primes a plant to acquire thermotolerance, which allows subsequent survival of more severe HS conditions. Acquired thermotolerance is actively maintained over several days (HS memory) and involves the sustained induction of memory-related genes. Here we show that FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) is specifically required for physiological HS memory and maintaining high memory-gene expression during the days following a HS exposure. HSFA3 mediates HS memory by direct transcriptional activation of memory-related genes after return to normal growth temperatures. HSFA3 binds HSFA2, and in vivo both proteins form heteromeric complexes with additional HSFs. Our results indicate that only complexes containing both HSFA2 and HSFA3 efficiently promote transcriptional memory by positively influencing histone H3 lysine 4 (H3K4) hyper-methylation. In summary, our work defines the major HSF complex controlling transcriptional memory and elucidates the in vivo dynamics of HSF complexes during somatic stress memory.

Highlights

Adaptive plasticity in stress responses is a key element of plant survival strategies
The immediate heat stress (HS) responses - as assayed by basal thermotolerance and acquired thermotolerance - were not affected in fgt[3] (Supplementary Fig. 1b-c)
We show that HSFA3 is required for sustained induction of several HS memory-related genes through direct gene activation and recruitment of histone H3K4 hypermethylation

Summary

Introduction

Adaptive plasticity in stress responses is a key element of plant survival strategies. Somatic transcriptional memory based on enhanced re-induction of stress-induced genes following a second stress exposure has been reported for drought stress[9,10], salt stress[11] and for defense-related priming[12,13,14] In these cases chromatin modifications, in particular histone H3 lysine 4 (H3K4) methylation have been correlated with transcriptional memory[9,11,12,13]. In nature, HS is often recurring, and plants can be primed by one HS for an improved response to a recurring HS after a stress-less lag phase of several days[3,21,22] This HS memory is an active process as it is genetically separable from the acquisition of thermotolerance, and several genes have been identified that function in HS memory[21,22,23,24,25]. FGT1 encodes the A. thaliana orthologue of Drosophila strawberry notch, a highly conserved helicase protein that is required to maintain an open chromatin conformation through cooperation with chromatin remodeling complexes of the SWI/ SNF family[24,36]

Methods

Results

Conclusion