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

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.

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A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory

The EMBO Journal ◽

10.15252/embj.201592593 ◽

2015 ◽

Vol 35 (2) ◽

pp. 162-175 ◽

Cited By ~ 111

Author(s):

Jörn Lämke ◽

Krzysztof Brzezinka ◽

Simone Altmann ◽

Isabel Bäurle

Keyword(s):

Heat Shock ◽

Histone Methylation ◽

Heat Shock Factor ◽

Stress Memory ◽

Transcriptional Stress ◽

Hit And Run

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Enterobacter sp. SA187 mediates plant thermotolerance by chromatin modification of heat stress genes

10.1101/2020.01.16.908756 ◽

2020 ◽

Author(s):

Kirti Shekhawat ◽

Arsheed Sheikh ◽

Kiruthiga Mariappan ◽

Rewaa Jalal ◽

Heribert Hirt

Keyword(s):

Global Warming ◽

Transcription Factors ◽

Heat Stress ◽

Crop Production ◽

Chromatin Modification ◽

Extreme Temperature ◽

Endophytic Bacterium ◽

Beneficial Microbes ◽

Stress Memory ◽

Stress Genes

AbstractGlobal warming has become a critical challenge to food safety, causing severe yield losses of major crops worldwide. Heat acclimation empowers plants to survive under extreme temperature conditions but the potential of beneficial microbes to make plants thermotolerant has not been considered so far. Here, we report that the endophytic bacterium Enterobacter sp. SA187 induces heat tolerance in Arabidopsis thaliana by reprogramming the plant transcriptome to a similar extent as acclimation. Acclimation induces priming of heat stress memory genes such as APX2 and HSP18.2 via the transcription factors HSFA1A, B, D, and E and the downstream master regulator HSFA2. hsfa1a,b,d,e and hsfa2 mutants compromised both acclimation and bacterial priming through the same pathway of HSF transcription factors. However, while acclimation transiently modifies H3K4me3 levels at heat stress memory gene loci, SA187 induces the constitutive priming of these loci. In summary, we demonstrate the molecular mechanism by which SA187 imparts thermotolerance in A. thaliana, suggesting that beneficial microbes might be a promising way to enhance crop production under global warming conditions.

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Light affects salt stress-induced transcriptional memory ofP5CS1inArabidopsis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1610670114 ◽

2016 ◽

Vol 113 (51) ◽

pp. E8335-E8343 ◽

Cited By ~ 42

Author(s):

Xuan Jun Feng ◽

Jing Rui Li ◽

Shi Lian Qi ◽

Qing Fang Lin ◽

Jing Bo Jin ◽

...

Keyword(s):

Salt Stress ◽

Higher Plants ◽

Light Exposure ◽

Environmental Stresses ◽

Proline Accumulation ◽

Metabolic Adaptation ◽

Recovery Stage ◽

Stress Memory ◽

Memory Response ◽

Transcriptional Memory

To cope with environmental stresses, plants often adopt a memory response upon primary stress exposure to facilitate a quicker and stronger reaction to recurring stresses. However, it remains unknown whether light is involved in the manifestation of stress memory. Proline accumulation is a striking metabolic adaptation of higher plants during various environmental stresses. Here we show that salinity-induced proline accumulation is memorable and HY5-dependent light signaling is required for such a memory response. Primary salt stress induced the expression of Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1), encoding a proline biosynthetic enzyme and proline accumulation, which were reduced to basal level during the recovery stage. Reoccurring salt stress-induced strongerP5CS1expression and proline accumulation were dependent upon light exposure during the recovery stage. Further studies demonstrated that salt-induced transcriptional memory ofP5CS1is associated with the retention of increased H3K4me3 level atP5CS1during the recovery stage. HY5 binds directly to light-responsive element, C/A-box, in theP5CS1promoter. Deletion of the C/A-box orhy5 hyhmutations caused rapid reduction of H3K4me3 level atP5CS1during the recovery stage, resulting in impairment of the stress memory response. These results unveil a previously unrecognized mechanism whereby light regulates salt-induced transcriptional memory via the function of HY5 in maintaining H3K4me3 level at the memory gene.

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

Nature Communications ◽

10.1038/s41467-021-23786-6 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Thomas Friedrich ◽

Vicky Oberkofler ◽

Inês Trindade ◽

Simone Altmann ◽

Krzysztof Brzezinka ◽

...

Keyword(s):

Heat Stress ◽

Stress Responses ◽

Transcriptional Activation ◽

Normal Growth ◽

Survival Strategies ◽

Adaptive Plasticity ◽

Stress Memory ◽

Transcriptional Memory ◽

Somatic Stress

AbstractAdaptive 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.

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Two cDNAs for Tomato Heat Stress Transcription Factors

PLANT PHYSIOLOGY ◽

10.1104/pp.102.4.1355 ◽

1993 ◽

Vol 102 (4) ◽

pp. 1355-1356 ◽

Cited By ~ 20

Author(s):

K. D. Scharf ◽

S. Rose ◽

J. Thierfelder ◽

L. Nover

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Heat Stress Transcription Factors

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Differential Expression of Heat Shock Transcription Factors and Heat Shock Proteins after Acute and Chronic Heat Stress in Laying Chickens (Gallus gallus)

PLoS ONE ◽

10.1371/journal.pone.0102204 ◽

2014 ◽

Vol 9 (7) ◽

pp. e102204 ◽

Cited By ~ 47

Author(s):

Jingjing Xie ◽

Li Tang ◽

Lin Lu ◽

Liyang Zhang ◽

Lin Xi ◽

...

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Heat Shock ◽

Heat Shock Proteins ◽

Differential Expression ◽

Gallus Gallus ◽

Heat Shock Transcription Factors ◽

Shock Proteins

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Characterization of novel regulators for heat stress tolerance in tomato from Indian sub-continent

10.1101/800607 ◽

2019 ◽

Author(s):

Sonia Balyan ◽

Sombir Rao ◽

Sarita Jha ◽

Chandni Bansal ◽

Jaishri Rubina Das ◽

...

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Functional Characterization ◽

Transcriptome Profiling ◽

Negative Regulator ◽

Comparative Transcriptome ◽

Regulatory Pathways ◽

Cool Region ◽

Promoter Swapping

AbstractThe footprint of tomato cultivation, a cool region crop that exhibits heat stress (HS) sensitivity, is increasing in the tropics/sub-tropics. Knowledge of novel regulatory hot-spots from varieties growing in the Indian sub-continent climatic zones could be vital for developing HS-resilient crops. Comparative transcriptome-wide signatures of a tolerant (CLN1621L) and sensitive (CA4) cultivar-pair short-listed from a pool of varieties exhibiting variable thermo-sensitivity using physiological, survival and yield-related traits revealed redundant to cultivar-specific HS-regulation with more up-regulated genes for CLN1621L than CA4. The anatgonisiticly-expressing genes include enzymes; have roles in plant defense and response to different abiotic stresses. Functional characterization of three antagonistic genes by overexpression and TRV-VIGS silencing established Solyc09g014280 (Acylsugar acyltransferase) and Solyc07g056570 (Notabilis), that are up-regulated in tolerant cultivar, as positive regulators of HS-tolerance and Solyc03g020030 (Pin-II proteinase inhibitor), that is down-regulated in CLN1621L, as negative regulator of thermotolerance. Transcriptional assessment of promoters of these genes by SNPs in stress-responsive cis-elements and promoter swapping experiments in opposite cultivar background showed inherent cultivar-specific orchestration of transcription factors in regulating transcription. Moreover, overexpression of three ethylene response transcription factors (ERF.C1/F4/F5) also improved HS-tolerance in tomato. This study identifies several novel HS-tolerance genes and provides proof of their utility in tomato-thermotolerance.HighlightNovel heat stress regulatory pathways uncovered by comparative transcriptome profiling between contrasting tomato cultivars from Indian sub-continent for improving thermotolerance. (20/30)

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