Heat Stress Phenotypes of Arabidopsis Mutants Implicate Multiple Signaling Pathways in the Acquisition of Thermotolerance

Larkindale, Jane; Hall, Jennifer; Knight, Marc R.; Vierling, Elizabeth

doi:10.1104/pp.105.062257

Cited by 757 publications

(690 citation statements)

References 64 publications

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“…Over the past few years, a more general role for SA as a mediator of diverse stress responses has been emerging. For example, in Arabidopsis SA is synthesized in response to abiotic stresses such as UV-C (30), ozone (31), cold (32), and heat (33,34) and has been shown to play a role in stress-induced developmental transitions, including flowering (35) and senescence (36). Although AtICS1 has been confirmed to be involved in many of these processes, it has only been implicated in others, such as cold-tolerant growth.…”

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confidence: 99%

Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses

Strawn

Marr

Inoue

et al. 2007

Journal of Biological Chemistry

219

146

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Salicylic acid (SA) is a phytohormone best known for its role in plant defense. It is synthesized in response to diverse pathogens and responsible for the large scale transcriptional induction of defense-related genes and the establishment of systemic acquired resistance. Surprisingly, given its importance in plant defense, an understanding of the underlying enzymology is lacking. In Arabidopsis thaliana, the pathogen-induced accumulation of SA requires isochorismate synthase (AtICS1). Here, we show that AtICS1 is a plastid-localized, stromal protein using chloroplast import assays and immunolocalization. AtICS1 acts as a monofunctional isochorismate synthase (ICS), catalyzing the conversion of chorismate to isochorismate (IC) in a reaction that operates near equilibrium (K eq ‫؍‬ 0.89). It does not convert chorismate directly to SA (via an IC intermediate) as does Yersinia enterocolitica Irp9. Using an irreversible coupled spectrophotometric assay, we found that AtICS1 exhibits an apparent K m of 41.5 M and k cat ‫؍‬ 38.7 min ؊1 for chorismate. This affinity for chorismate would allow it to successfully compete with other pathogen-induced, chorismate-utilizing enzymes. Furthermore, the biochemical properties of AtICS1 indicate its activity is not regulated by light-dependent changes in stromal pH, Mg 2؉ , or redox and that it is remarkably active at 4°C consistent with a role for SA in cold-tolerant growth. Finally, our analyses support plastidic synthesis of stress-induced SA with the requirement for one or more additional enzymes responsible for the conversion of IC to SA, because non-enzymatic conversion of IC to SA under physiological conditions was negligible.

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confidence: 99%

Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses

Strawn

Marr

Inoue

et al. 2007

Journal of Biological Chemistry

219

146

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“…Arabidopsis contains 21 different HSF genes (27), and this high multiplicity suggests the importance of backup and diversification of HSFs. However, microarray and genetic data indicate that different regulatory systems contribute to heat tolerance at different stages of the plant life cycle, and that different gene sets may control the complex multigenic process for acquiring thermotolerance (28,29).…”

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confidence: 99%

Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression

Sakuma

Maruyama²,

Qin³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

708

590

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Transcription factor DREB2A interacts with a cis-acting dehydration-responsive element (DRE) sequence and activates expression of downstream genes involved in drought-and salt-stress response in Arabidopsis thaliana. Intact DREB2A expression does not activate downstream genes under normal growth conditions. A negative regulatory domain exists in the central region of DREB2A, and deletion of this region transforms DREB2A to a constitutive active form (DREB2A CA). We carried out microarray analysis of transgenic Arabidopsis-overexpressing DREB2A CA and found that the overexpression of DREB2A CA induces not only drought-and salt-responsive genes but also heat-shock (HS)-related genes. Moreover, we found that transient induction of the DREB2A occurs rapidly by HS stress, and that the sGFP-DREB2A protein accumulates in nuclei of HS-stressed cells. DREB2A up-regulated genes were classified into three groups based on their expression patterns: genes induced by HS, genes induced by drought stress, and genes induced by both HS and drought stress. DREB2A up-regulated genes were down-regulated in DREB2A knockout mutants under stress conditions. Thermotolerance was significantly increased in plants overexpressing DREB2A CA and decreased in DREB2A knockout plants. Collectively, these results indicate that DREB2A functions in both water and HS-stress responses.AP2-type transcription factor ͉ drought-stress tolerance ͉ heat-stress tolerance ͉ knockout mutants ͉ microarray analysis

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“…Thermotolerance is an essential component of the acclimation response of different organisms (1)(2)(3)(4)(5)(6). It is generally divided into acquired thermotolerance (i.e.…”

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confidence: 99%

The Transcriptional Co-activator MBF1c Is a Key Regulator of Thermotolerance in Arabidopsis thaliana

Suzuki

Bajad

Shuman

et al. 2008

Journal of Biological Chemistry

262

241

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The ability of an organism to acclimate to its environment is a key determinant in its global distribution and capacity to compete with other organisms. The heat stress response, a highly conserved environmental and developmental program in eukaryotic and prokaryotic organisms, is an important component of the acclimation response of plants. Previous studies have shown that heat shock transcription factors play an important role in thermotolerance in plants and other organisms, controlling the expression of different heat shock proteins and detoxifying enzymes. In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, were recently shown to play a central role in thermotolerance in plants, a key regulator of these responses was not identified. Here we report that the highly conserved transcriptional coactivator, MBF1c (multiprotein bridging factor 1c), is a key regulator of thermotolerance in Arabidopsis thaliana. MBF1c protein accumulates rapidly and is localized to nuclei during heat stress. MBF1c is required for thermotolerance and functions upstream to SA, trehalose, ethylene, and pathogenesis-related protein 1 during heat stress. In contrast, MBF1c is not required for the expression of transcripts encoding HSFA2 and different heat shock proteins. Interestingly, MBF1c interacts with TPS5 (trehalose phosphate synthase 5), which is also heat-inducible, and mutants deficient in TPS5 are thermosensitive. Our results provide evidence for the existence of a tightly coordinated heat stress-response network, involving trehalose-, SA-, and ethylene-signaling pathways, that is under the control of MBF1c.Thermotolerance is an essential component of the acclimation response of different organisms (1-6). It is generally divided into acquired thermotolerance (i.e. the ability to acquire tolerance to otherwise lethal heat stress) and basal thermotolerance (i.e. the inherent ability to survive temperature above the optimal growth) (5). Previous studies have shown that heat shock transcription factors (HSFs) 2 play an important role in thermotolerance in plants and other organisms, regulating heat shock proteins (HSPs) as well as different acclimation and detoxification proteins (7-10). In contrast, although several other pathways, involving ethylene, salicylic acid (SA), and trehalose, have recently been proposed to play an important role in thermotolerance in plants (5, 11-15), a key regulator of these responses was not identified.MBF1 (multiprotein bridging factor 1) is a highly conserved transcriptional co-activator involved in the regulation of diverse processes, such as endothelial cell differentiation, hormone-regulated lipid metabolism, central nervous system development, and histidine metabolism (16 -19). MBF1 proteins from different organisms interact with transcription factors, such as c-Jun, GCN4, and ATF1, or with different hormone receptors and link them with the TATA-binding protein (16 -20). The flowering plant Arabidopsis thaliana contains three different genes e...

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Heat Stress Phenotypes of Arabidopsis Mutants Implicate Multiple Signaling Pathways in the Acquisition of Thermotolerance

Cited by 757 publications

References 64 publications

Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses

Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses

Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression

The Transcriptional Co-activator MBF1c Is a Key Regulator of Thermotolerance in Arabidopsis thaliana

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