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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.

SUBMITTER: Friedrich T

PROVIDER: S-EPMC8187452 | biostudies-literature |

REPOSITORIES: biostudies-literature

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

Project description: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. We find FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) to be 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 promoting 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.

2021-05-04 | GSE162434 | GEO

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

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

| PRJNA681862 | ENA

Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2.

Project description:So far little is known on the functional role of phosphorylation in the heat stress response of plants. Here we present evidence that heat stress activates the Arabidopsis mitogen-activated protein kinase MPK6. In vitro and in vivo evidence is provided that MPK6 specifically targets the major heat stress transcription factor HsfA2. Activation of MPK6 results in complex formation with HsfA2. MPK6 phosphorylates HsfA2 on T249 and changes its intracellular localisation. Protein kinase and phosphatase inhibitor studies indicate that HsfA2 protein stability is regulated in a phosphorylation-dependent manner, but this mechanism is independent of MPK6. Overall, our data show that heat stress-induced targeting of HsfA2 by MPK6 participates in the complex regulatory mechanism how plants respond to heat stress.

| S-EPMC3628891 | biostudies-literature

CSN5A Subunit of COP9 Signalosome Is Required for Resetting Transcriptional Stress Memory after Recurrent Heat Stress in Arabidopsis.

Project description:In nature, plants are exposed to several environmental stresses that can be continuous or recurring. Continuous stress can be lethal, but stress after priming can increase the tolerance of a plant to better prepare for future stresses. Reports have suggested that transcription factors are involved in stress memory after recurrent stress; however, less is known about the factors that regulate the resetting of stress memory. Here, we uncovered a role for Constitutive Photomorphogenesis 5A (CSN5A) in the regulation of stress memory for resetting transcriptional memory genes (APX2 and HSP22) and H3K4me3 following recurrent heat stress. Furthermore, CSN5A is also required for the deposition of H3K4me3 following recurrent heat stress. Thus, CSN5A plays an important role in the regulation of histone methylation and transcriptional stress memory after recurrent heat stress.

| S-EPMC8146153 | biostudies-literature

The mediator kinase module enhances polymerase activity to regulate transcriptional memory after heat stress in Arabidopsis

Project description:Plants are often exposed to recurring adverse environmental conditions in the wild. Acclimation to high temperatures entails transcriptional responses, which prime plants to better withstand subsequent stress events. Heat stress (HS)-induced transcriptional memory results in more efficient re-induction of transcription upon recurrence of heat stress. Here, we identified CDK8 and MED12, two subunits of the kinase module of the transcription co-regulator complex, mediator, as promoters of heat stress memory and associated histone modifications in Arabidopsis. CDK8 is recruited to heat-stress memory genes by HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2). Like HSFA2, CDK8 is largely dispensable for the initial gene induction upon heat stress, and its function in transcriptional memory is thus independent of primary gene activation. In addition to the promoter and transcriptional start region of target genes, CDK8 also binds their 3ʹ-region, where it may promote elongation, termination, or rapid re-initiation of RNA polymerase II (Pol II) complexes during transcriptional memory bursts. Our work presents a complex role for the mediator kinase module during transcriptional memory in multicellular eukaryotes, through interactions with transcription factors, chromatin modifications, and promotion of Pol II efficiency.

| S-SCDT-10_1038-S44318-023-00024-X | biostudies-other

Coordination between bZIP28 and HSFA2 in the regulation of heat response signals in Arabidopsis.

Project description:Heat stress can have detrimental effects on yield production worldwide. Although bZIP28 and HSFA2 were identified as putative heat sensors in plants, coordination between them has not been uncovered. In this study, the deficiency in bZIP28 did not affect heat tolerance in plants. However, the plants lacking bZIP28 showed enhanced activation of APXs-, MBF1c-and HSPs-dependent pathways as well as higher level of HsfA2 transcripts and H2O2 accumulation, suggesting that these pathways might compensate for the deficiency in bZIP28 during heat stress. In addition, requirement of HSFA2 for the activation of APXs-dependent pathway during heat stress was supported by the analyses of plants lacking HSFA2. Our study demonstrated the flexible mode of heat response pathways involving bZIP28, HSFA2 and ROS-dependent signals.

| S-EPMC5703228 | biostudies-literature

Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers.

Project description:The high sensitivity of male reproductive cells to high temperatures may be due to an inadequate heat stress response. The results of a comprehensive expression analysis of HsfA2 and Hsp17-CII, two important members of the heat stress system, in the developing anthers of a heat-tolerant tomato genotype are reported here. A transcriptional analysis at different developmental anther/pollen stages was performed using semi-quantitative and real-time PCR. The messengers were localized using in situ RNA hybridization, and protein accumulation was monitored using immunoblot analysis. Based on the analysis of the gene and protein expression profiles, HsfA2 and Hsp17-CII are finely regulated during anther development and are further induced under both short and prolonged heat stress conditions. These data suggest that HsfA2 may be directly involved in the activation of protection mechanisms in the tomato anther during heat stress and, thereby, may contribute to tomato fruit set under adverse temperatures.

| S-EPMC2803211 | biostudies-literature

Transcriptomic analysis of heat stress transcriptional memory in Arabidopsis seedling

Project description:Plants can be primed by a stress cue to mount a faster and stronger activation of defense mechanisms upon a subsequent stress. A crucial component of such stress priming is the modified reactivation of genes upon recurring stress, a phenomenon known as transcriptional memory. The transcriptional memory in response to heat stress is not clear at the genome scale. We used microarrays to identify genes that showed transcriptional memory in response to recurring heat stress.

2018-07-09 | GSE103398 | GEO

Memory of 5-min heat stress in <i>Arabidopsis thaliana</i>.

Project description:An ability of plants memorizing past heat exposure to modulate the expression of stress response transcripts during recovery is essential for efficient acquired thermotolerance. In this study, we demonstrated that expression of heat response transcripts spiked at 30 min or 1 h, but dramatically declined at 3 h during recoveries following exposure to 5-min heat stress in Arabidopsis. In contrast, expression of transcripts up-regulated by 45-min heat stress was sustained for 30 min or 1 h then declined during recovery. These results suggest that heat memory can be differently modulated depending on the duration of heat exposure, and indicate that plants can memorize even 5-min heat stress to regulate acclimatory responses during recovery. Later hypothesis can be supported by the finding that accumulation of heat response proteins was also modulated during recovery following 5-min heat stress. In addition, 5-min heat stress followed by 3 h recovery was efficient to activate acquired thermotolerance of plants, although spike of transcript expression was observed at 1 h during recovery. These results suggest that plants possess the ability to quickly memorize heat stress and reset cellular states during recovery to adapt to subsequent severe heat stress.

| S-EPMC8570703 | biostudies-literature

Specific interaction between tomato HsfA1 and HsfA2 creates hetero-oligomeric superactivator complexes for synergistic activation of heat stress gene expression.

Project description:In plants, a family of more than 20 heat stress transcription factors (Hsf) controls the expression of heat stress (hs) genes. There is increasing evidence for the functional diversification between individual members of the Hsf family fulfilling distinct roles in response to various environmental stress conditions and developmental signals. In response to hs, accumulation of both heat stress proteins (Hsp) and Hsfs is induced. In tomato, the physical interaction between the constitutively expressed HsfA1 and the hs-inducible HsfA2 results in synergistic transcriptional activation (superactivation) of hs gene expression. Here, we show that the interaction is strikingly specific and not observed with other class A Hsfs. Hetero-oligomerization of the two-component Hsfs is preferred to homo-oligomerization, and each Hsf in the HsfA1/HsfA2 hetero-oligomeric complex has its characteristic contribution to its function as superactivator. Distinct regions of the oligomerization domain are responsible for specific homo- and hetero-oligomeric interactions leading to the formation of hexameric complexes. The results are summarized in a model of assembly and function of HsfA1/A2 superactivator complexes in hs gene regulation.

| S-EPMC2742850 | biostudies-other

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