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

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.

The Epigenetic Mechanisms Underlying Thermomorphogenesis and Heat Stress Responses in Arabidopsis

“…Interestingly, chromatin immunoprecipitation analysis demonstrated a significant depletion in global deposition of H3K9me2 and H3K4me3 repressing marks in Arabidopsis plants subjected to prolonged heat stress treatments [40]. As mentioned in the introduction, an important HSF factor, HSFA2, forms heterodimers with HSFA3 and interacts with additional HSFs to recruit H3K4 histone methyltransferases and mediate histone H3K4 hypermethylation to maintain transcriptional memory during HS recovery [44,45] (Figure 2). In recent years, a lot of effort has been made to elucidate the role of histone acetylation in mediating heat stress-induced responses.…”

“…Plant adaptation to heat stress also relies on a number of epigenetic mechanisms, including chromatin remodeling, chromatin-associated SUMOylation [26], histone modifications [40,[44][45][46][47][48][49][50] and ncRNA regulation [60]. Although a lot of effort has been put on elucidating the epigenetic adaptation to heat acclimation, the current literature is still lacking evidence on how different factors such as transcription factors, ncRNAs and chromatin modifications cooperate to configure heat stress responses.…”

Epigenetic regulation of thermomorphogenesis and heat stress tolerance

“…5b), suggesting a recent event of transcriptional activation (Ng et al ., 2004; D’Urso et al ., 2016). Moreover, H3K4 hypermethylation contributes to the priming of gene expression in HS and to pathogen defence responses (Jaskiewicz et al ., 2011; Mozgova et al ., 2015; Friedrich et al ., 2021). Strikingly, H3K4 methylation has a role in cold signalling and vernalisation as well (reviewed in Luo & He, 2020; Pandey et al ., 2021).…”

“…Emerging research from the last few years indicated that HS memory is partly based on epigenetic mechanisms. In Arabidopsis, at the whole plant level, HS memory lasts for up to 5 d and results in increased survival after a HS that is lethal to a naïve (nonprimed) plant (Charng et al ., 2006; Stief et al ., 2014; Friedrich et al ., 2021). At the level of gene expression, this is reflected by two types of transcriptional memory (Fig.…”

Molecular Bases of Heat Stress Responses in Vegetable Crops With Focusing on Heat Shock Factors and Heat Shock Proteins

“…Strong/rapid expression of sHSP genes including HSP21 , HSP22 , and HSP17.6C is observed in primed plants compared to non-primed plants ( Yamaguchi et al, 2021 ). FORGETTER3 ( FGT3 )/ HSFA3 is needed to retain HS memory for several days following HS exposure ( Friedrich et al, 2021 ). A recent discovery showed that genes encoding stem cell regulators such as CLAVATA1 ( CLV1 ), CLV3 , and HSP17.6A , and the primary carbohydrate metabolism gene FRUCTOSE-BISPHOSPHATE ALDOLASE 6 ( FBA6 ) are involved in the HS transcriptional memory in the shoot apical meristem ( Olas et al, 2021 ).…”