HsfA7 coordinates the transition from mild to strong heat stress response by controlling the activity of the master regulator HsfA1a in tomato

Mesihovic, Anida; Ullrich, Sarah; Rosenkranz, Remus; Gebhardt, Philipp; Bublak, Daniela; Eich, Hannah; Weber, Daniel; Berberich, Thomas; Scharf, Klaus‐Dieter; Schleiff, Enrico; Fragkostefanakis, Sotirios

doi:10.1016/j.celrep.2021.110224

Cited by 23 publications

(28 citation statements)

References 44 publications

(64 reference statements)

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“…HsfA1a is a constitutively expressed gene mainly regulated at posttranslational level (El-shershaby et al 2019;Mesihovic et al 2022). We also confirmed that HsfA1a transcript levels do not significantly change in response to TUN treatment (Supplemental Fig.…”

Section: Effect Of Hsfa1a Overexpression or Suppression On The Tolera...supporting

confidence: 78%

Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato

Löchli

Torbica

Haile-Weldeslasie

et al. 2023

Cell Stress and Chaperones

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Conditions that cause proteotoxicity like high temperature trigger the activation of unfolded protein response (UPR). The cytosolic (CPR) and endoplasmic reticulum (ER) UPR rely on heat stress transcription factor (HSF) and two members of the basic leucine zipper (bZIP) gene family, respectively. In tomato, HsfA1a is the master regulator of CPR. Here, we identified the core players of tomato ER-UPR including the two central transcriptional regulators, namely bZIP28 and bZIP60. Interestingly, the induction of ER-UPR genes and the activation of bZIP60 are altered in transgenic plants where HsfA1a is either overexpressed (A1aOE) or suppressed (A1CS), indicating an interplay between CPR and ER-UPR systems. Several ER-UPR genes are differentially expressed in the HsfA1a transgenic lines either exposed to heat stress or to the ER stress elicitor tunicamycin (TUN). The ectopic expression of HsfA1a is associated with higher tolerance against TUN. On the example of the ER-resident Hsp70 chaperone BIP3, we show that the presence of cis-elements required for HSF and bZIP regulation serves as a putative platform for the co-regulation of these genes by both CPR and ER-UPR mechanisms, in the case of BIP3 in a stimulatory manner under high temperatures. In addition, we show that the accumulation of HsfA1a results in higher levels of three ATG genes and a more sensitized induction of autophagy in response to ER stress which also supports the increased tolerance to ER stress of the A1aOE line. These findings provide a basis for the coordination of protein homeostasis in different cellular compartments under stress conditions.

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Section: Effect Of Hsfa1a Overexpression or Suppression On The Tolera...supporting

confidence: 78%

Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato

Löchli

Torbica

Haile-Weldeslasie

et al. 2023

Cell Stress and Chaperones

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“…Cultivated tomatoes have large apical bud structure which may affect meristem temperature, which has been thought to be drastically impacted by apical bud structure and function [ 53 ]. Since HsfA7 is a capacitor of the central regulator of HsfA1 during the early heat stress response [ 50 ], its distinctive expression response may be caused by the putative difference in meristem temperature between Moneymaker and its ancestral relatives. Notably, plant temperature is one of the key modulators controlling plant development and heat stress transcription factors (i.e., HSFA2 in Arabidopsis) have been shown to regulate heat stress-related SAM development [ 54 , 55 ].…”

Section: Discussionmentioning

confidence: 99%

“…To breed new varieties suitable for growing in suboptimal environments under the current trend of global climate change, it is important to understand how domestication and breeding has changed phenotypic plasticity. Notably, recent studies have revealed that gene expression regulated by AS plays crucial roles in plant response to changing environments, especially varying temperature [ 26 , 30 , 46 , 47 , 48 , 49 , 50 ]. In tomatoes, intronic polymorphisms affecting AS of the heat stress transcription factor HsfA2 have been found to be associated with the difference in heat stress response between cultivated tomato and wild species [ 51 ].…”

Section: Introductionmentioning

confidence: 99%

Comparative Analysis of Environment-Responsive Alternative Splicing in the Inflorescences of Cultivated and Wild Tomato Species

Zhou

Wang

Weng

et al. 2022

IJMS

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Cultivated tomato (Solanum lycopersicum) is bred for fruit production in optimized environments, in contrast to harsh environments where their ancestral relatives thrive. The process of domestication and breeding has profound impacts on the phenotypic plasticity of plant development and the stress response. Notably, the alternative splicing (AS) of precursor message RNA (pre-mRNA), which is one of the major factors contributing to transcriptome complexity, is responsive to developmental cues and environmental change. To determine a possible association between AS events and phenotypic plasticity, we investigated environment-responsive AS events in the inflorescences of cultivated tomato and its ancestral relatives S. pimpinellifolium. Despite that similar AS frequencies were detected in the cultivated tomato variety Moneymaker and two S. pimpinellifolium accessions under the same growth conditions, 528 genes including splicing factors showed differential splicing in the inflorescences of plants grown in open fields and plastic greenhouses in the Moneymaker variety. In contrast, the two S. pimpinellifolium accessions, LA1589 and LA1781, had 298 and 268 genes showing differential splicing, respectively. Moreover, seven heat responsive genes showed opposite expression patterns in response to changing growth conditions between Moneymaker and its ancestral relatives. Accordingly, there were eight differentially expressed splice variants from genes involved in heat response in Moneymaker. Our results reveal distinctive features of AS events in the inflorescences between cultivated tomato and its ancestral relatives, and show that AS regulation in response to environmental changes is genotype dependent.

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“…Therefore, the acclimation of tomato to HS is dependent on the AS of HsfA2 ( Hu et al, 2020b ). Worth mentioning, tomato HsfA7 is subjected to the same regulatory control like HsfA2, further highlighting the important of AS for thermotolerance ( Mesihovic et al, 2022 ).…”

Section: Gene-specific Studies Showcasing the Significance Of Alterna...mentioning

confidence: 99%

Relevance and Regulation of Alternative Splicing in Plant Heat Stress Response: Current Understanding and Future Directions

et al. 2022

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Alternative splicing (AS) is a major mechanism for gene expression in eukaryotes, increasing proteome diversity but also regulating transcriptome abundance. High temperatures have a strong impact on the splicing profile of many genes and therefore AS is considered as an integral part of heat stress response. While many studies have established a detailed description of the diversity of the RNAome under heat stress in different plant species and stress regimes, little is known on the underlying mechanisms that control this temperature-sensitive process. AS is mainly regulated by the activity of splicing regulators. Changes in the abundance of these proteins through transcription and AS, post-translational modifications and interactions with exonic and intronic cis-elements and core elements of the spliceosomes modulate the outcome of pre-mRNA splicing. As a major part of pre-mRNAs are spliced co-transcriptionally, the chromatin environment along with the RNA polymerase II elongation play a major role in the regulation of pre-mRNA splicing under heat stress conditions. Despite its importance, our understanding on the regulation of heat stress sensitive AS in plants is scarce. In this review, we summarize the current status of knowledge on the regulation of AS in plants under heat stress conditions. We discuss possible implications of different pathways based on results from non-plant systems to provide a perspective for researchers who aim to elucidate the molecular basis of AS under high temperatures.

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HsfA7 coordinates the transition from mild to strong heat stress response by controlling the activity of the master regulator HsfA1a in tomato

Cited by 23 publications

References 44 publications

Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato

Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato

Comparative Analysis of Environment-Responsive Alternative Splicing in the Inflorescences of Cultivated and Wild Tomato Species

Relevance and Regulation of Alternative Splicing in Plant Heat Stress Response: Current Understanding and Future Directions

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