Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation

Charng, Yuh-Chyang; Liu, Hsiang-chin; Liu, Nai-yu; Hsu, Fu-Chiun; Ko, Swee-Suak

doi:10.1104/pp.105.074898

Cited by 258 publications

(244 citation statements)

References 41 publications

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“…The Arabidopsis (Arabidopsis thaliana) T-DNA KO mutants hsp101, hot1-3, and hsa32-1 were as described previously (Lee et al, 2005;Charng et al, 2006). The double KO mutant hsp101 hsa32-1 was generated by crossing the single mutant lines and isolated from the offspring in the F2 generation.…”

Section: Plants Materials and Mutant Screenmentioning

confidence: 99%

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Interplay between Heat Shock Proteins HSP101 and HSA32 Prolongs Heat Acclimation Memory Posttranscriptionally in Arabidopsis

Juan

Hsu

et al. 2013

Plant Physiology

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Heat acclimation improves the tolerance of organisms to severe heat stress. Our previous work showed that in Arabidopsis (Arabidopsis thaliana), the "memory" of heat acclimation treatment decayed faster in the absence of the heat-stress-associated 32-kD protein HSA32, a heat-induced protein predominantly found in plants. The HSA32 null mutant attains normal short-term acquired thermotolerance but is defective in long-term acquired thermotolerance. To further explore this phenomenon, we isolated Arabidopsis defective in long-term acquired thermotolerance (dlt) mutants using a forward genetic screen. Two recessive missense alleles, dlt1-1 and dlt1-2, encode the molecular chaperone heat shock protein101 (HSP101). Results of immunoblot analyses suggest that HSP101 enhances the translation of HSA32 during recovery after heat treatment, and in turn, HSA32 retards the decay of HSP101. The dlt1-1 mutation has little effect on HSP101 chaperone activity and thermotolerance function but compromises the regulation of HSA32. In contrast, dlt1-2 impairs the chaperone activity and thermotolerance function of HSP101 but not the regulation of HSA32. These results suggest that HSP101 has a dual function, which could be decoupled by the mutations. Pulse-chase analysis showed that HSP101 degraded faster in the absence of HSA32. The autophagic proteolysis inhibitor E-64d, but not the proteasome inhibitor MG132, inhibited the degradation of HSP101. Ectopic expression of HSA32 confirmed its effect on the decay of HSP101 at the posttranscriptional level and showed that HSA32 was not sufficient to confer long-term acquired thermotolerance when the HSP101 level was low. Taken together, we propose that a positive feedback loop between HSP101 and HSA32 at the protein level is a novel mechanism for prolonging the memory of heat acclimation.

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Section: Plants Materials and Mutant Screenmentioning

confidence: 99%

“…However, just how plants keep the memory of heat acclimation is not clear. Our previous studies suggest that a heat-induced 32-kD protein, HSA32, is involved in prolonging the memory of heat acclimation in Arabidopsis (Arabidopsis thaliana; Charng et al, 2006). HSA32 is not a canonical heat shock protein (HSP).…”

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confidence: 99%

Interplay between Heat Shock Proteins HSP101 and HSA32 Prolongs Heat Acclimation Memory Posttranscriptionally in Arabidopsis

Juan

Hsu

et al. 2013

Plant Physiology

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“…Acquisition of thermotolerance has been found to be negatively affected in Hsp70 antisense A. thaliana plants ( Lee and Schoffl, 1996). Hsa32 in A. thaliana is heat-inducible protein (Charng et al, 2006). Mutant/ RNAi plants lacking Hsa32 do not survive a severe HS treatment even after a pre-treatment at a sublethal temperature (Charng et al, 2006).…”

Section: High Temperature Tolerant Transgenics Raised Through Alterinmentioning

confidence: 99%

“…Hsa32 in A. thaliana is heat-inducible protein (Charng et al, 2006). Mutant/ RNAi plants lacking Hsa32 do not survive a severe HS treatment even after a pre-treatment at a sublethal temperature (Charng et al, 2006). Very recently, Charng et al (2007) have shown that HsfA2 (heat-inducible trans-activator protein which sustains the expression of Hsp genes and prolongs the acquired thermotolerance in A. thaliana) under-expression results in an increased sensitivity of the mutant plants to HS.…”

Section: High Temperature Tolerant Transgenics Raised Through Alterinmentioning

confidence: 99%

Genetic engineering for heat tolerance in plants

Singh

Grover

2008

Physiol Mol Biol Plants

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High temperature tolerance has been genetically engineered in plants mainly by over-expressing the heat shock protein genes or indirectly by altering levels of heat shock transcription factor proteins. Apart from heat shock proteins, thermotolerance has also been altered by elevating levels of osmolytes, increasing levels of cell detoxification enzymes and through altering membrane fluidity. It is suggested that Hsps may be directly implicated in thermotolerance as agents that minimize damage to cell proteins. The other three above approaches leading to thermotolerance in transgenic experiments though operate in their own specific ways but indirectly might be aiding in creation of more reductive and energy-rich cellular environment, thereby minimizing the accumulation of damaged proteins. Intervention in protein metabolism such that accumulation of damaged proteins is minimized thus appears to be the main target for genetically-engineering crops against high temperature stress. High temperature-induced gene expression system is one of the best-studied model systems for analyzing induced gene expression. The molecular basis of heat shock (HS) response was revealed for the first time when Ritossa (1962) reported that temperature elevation brings about altered puffing pattern of polytene chromosomes in Drosophila. Tissieres et al. (1974) for the first time showed that the HS condition results in altered protein profile in the Drosophila cells. Further studies established that nearly all organisms, ranging from bacteria to man, respond to HS by synthesizing a new set of proteins called heat shock proteins (Hsp). The HS system has been investigated in great depth using diverse biological systems including microbes (e.g. Escherichia coli, Saccharomyces cerevisiae), animals (e.g. Drosophila melanogaster, Homo sapiens) and plants (e.g. Arabidopsis thaliana, Oryza sativa, Solanum lycopersicon) species. In recent years, detailed understanding has been gained on various components of the heat shock response (HSR) in living organisms including features like heat shock genes/proteins, heat shock promoters and heat shock elements (HSEs), heat shock factors (HSFs), possible receptors of the heat shock response, signaling components and chromatin remodeling aspects (Grover, 2002, Wahid et al., 2007.Plant scientists have a concern in altering the HS response as high ambient temperature is one of the major constraints in obtaining maximum output from the crop plants. Most crops are affected by daily fluctuations in high day and/or night temperatures. While some stages of plant growth may be more sensitive to high temperature than others, there is an overall reduction in plant performance when temperature is higher than the optimal temperature at specific growth stages. Conventional breeding for high temperature stress tolerance has not been much successful due to several reasons like lack of suitable source of genes in sexuallycompatible gene pools, complex nature of the HS trait, lack of understanding on the genetic mech...

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“…HSFA3 plays a key role in expression of many HSP genes, gene products of which contribute to either positive or negative feedback of heat stress responses and eventually provides efficient plant heat stress adaptation (Charng et al, 2006). Because mature mRNA expression of HSFA3 correlated well with plant heat tolerance in our two-step acquired heat assay, we further examined whether HSFA3 could drive plant heat stress tolerance for itself downstream of STA1.…”

Section: Reconstitution Of Heat-inducible Transcription Cascades By Dmentioning

confidence: 99%

STABILIZED1 Modulates Pre-mRNA Splicing for Thermotolerance

Kim

Cho

Lee³

et al. 2017

Plant Physiol.

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High-temperature stress often leads to differential RNA splicing, thus accumulating different types and/or amounts of mature mRNAs in eukaryotic cells. However, regulatory mechanisms underlying plant precursor mRNA (pre-mRNA) splicing in the environmental stress conditions remain elusive. Herein, we describe that a U5-snRNP-interacting protein homolog STABILIZED1 (STA1) has pre-mRNA splicing activity for heat-inducible transcripts including HEAT STRESS TRANSCRIPTION FACTORs and various HEAT SHOCK PROTEINs for the establishment of heat stress tolerance in Arabidopsis (Arabidopsis thaliana). Our cell-based splicing reporter assay demonstrated STA1 acts on pre-mRNA splicing for specific subsets of stressrelated genes. Cellular reconstitution of heat-inducible transcription cascades supported the view that STA1-dependent premRNA splicing plays a role in DREB2A-dependent HSFA3 expression for heat-responsive gene expression. Further genetic analysis with a loss-of-function mutant sta1-1, STA1-expressing transgenic plants in Col background, and STA1-expressing transgenic plants in the sta1-1 background verified that STA1 is essential in expression of necessary genes including HSFA3 for two-step heat stress tolerance in plants. However, constitutive overexpression of the cDNA version of HSFA3 in the sta1-1 background is unable to execute plant heat stress tolerance in sta1-1. Consistently our global target analysis of STA1 showed that its splicing activity modulates a rather broad range of gene expression in response to heat treatment. The findings of this study reveal that heat-inducible STA1 activity for pre-mRNA splicing serves as a molecular regulatory mechanism underlying the plant stress tolerance to high-temperature stress.The splicing of precursor mRNA (pre-mRNA) is a necessary step for intron-containing gene expression in eukaryotic cells to produce mature transcripts for protein translation (Wahl et al., 2009). This process is highly ordered and tightly controlled by multisubunit spliceosome activity to mix and match introns and exons of pre-mRNAs. The high molecular weight spliceosome complex comprises small nuclear ribonucleoprotein particles (snRNPs) called U1, U2, U4/U6, and U5 snRNPs. For splicing of pre-mRNA introns, U1 snRNP recognizes the 59-splicing site, and U2 snRNP binds to the adenosine at the branch point of introns with the assistance of U2 auxiliary factors. U4/U6 and U5 trimeric snRNPs associate with each other and undergo a stepwise 39-splicing site cleavage process. Eventually, U5 snRNP dissociates from the complex along with a lariat form of the intron. In this process, U5 snRNP accurately and dynamically swaps interacting partners with other snRNP subunits (Wahl et al., 2009).

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Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation

Cited by 258 publications

References 41 publications

Interplay between Heat Shock Proteins HSP101 and HSA32 Prolongs Heat Acclimation Memory Posttranscriptionally in Arabidopsis

Interplay between Heat Shock Proteins HSP101 and HSA32 Prolongs Heat Acclimation Memory Posttranscriptionally in Arabidopsis

Genetic engineering for heat tolerance in plants

STABILIZED1 Modulates Pre-mRNA Splicing for Thermotolerance

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