Expression of a monothiol glutaredoxin, AtGRXS17, in tomato (Solanum lycopersicum) enhances drought tolerance

Wu, Qingyu; Hu, Ying; Sprague, Stuart; Kakeshpour, Tayebeh; Park, Jungeun; Nakata, Paul A.; Cheng, Ninghui; Hirschi, Kendal D.; White, Frank F.; Park, Sunghun

doi:10.1016/j.bbrc.2017.08.006

Cited by 42 publications

(20 citation statements)

References 45 publications

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“…5a and c) indicated that knockout of SlNPR1 augmented oxidative damage caused by drought stress. Additionally, membrane damage is always caused by accumulation of ROS under drought stress [44], which is in agreement with the higher H 2 O 2 content observed in slnpr1 mutants (Fig. 5b).…”

Section: Discussionsupporting

confidence: 83%

CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance

et al. 2019

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BackgroundNPR1, nonexpressor of pathogenesis-related gene 1, is a master regulator involved in plant defense response to pathogens, and its regulatory mechanism in the defense pathway has been relatively clear. However, information about the function of NPR1 in plant response to abiotic stress is still limited. Tomato is the fourth most economically crop worldwide and also one of the best-characterized model plants employed in genetic studies. Because of the lack of a stable tomato NPR1 (SlNPR1) mutant, little is known about the function of SlNPR1 in tomato response to biotic and abiotic stresses.ResultsHere we isolated SlNPR1 from tomato ‘Ailsa Craig’ and generated slnpr1 mutants using the CRISPR/Cas9 system. Analysis of the cis-acting elements indicated that SlNPR1 might be involved in tomato plant response to drought stress. Expression pattern analysis showed that SlNPR1 was expressed in all plant tissues, and it was strongly induced by drought stress. Thus, we investigated the function of SlNPR1 in tomato-plant drought tolerance. Results showed that slnpr1 mutants exhibited reduced drought tolerance with increased stomatal aperture, higher electrolytic leakage, malondialdehyde (MDA) and hydrogen peroxide (H2O2) levels, and lower activity levels of antioxidant enzymes, compared to wild type (WT) plants. The reduced drought tolerance of slnpr1 mutants was further reflected by the down-regulated expression of drought related key genes, including SlGST, SlDHN, and SlDREB.ConclusionsCollectively, the data suggest that SlNPR1 is involved in regulating tomato plant drought response. These results aid in further understanding the molecular basis underlying SlNPR1 mediation of tomato drought sensitivity.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1627-4) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 83%

CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance

et al. 2019

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“…For instance, a putative glutaredoxin (Solyc06g008760) is downregulated in Red Setter at 45 °C. Glutaredoxins are important for redox regulation, which is essential for thermotolerance, and it has been previously shown that overexpression of an A. thaliana glutaredoxin enhances both drought and HS tolerance in tomato [ 56 , 57 ]. In contrast, Solyc01g081250, Solyc09g005420 and Solyc11g011010 are upregulated at 45 °C in Red Setter when compared to the other genotypes.…”

Section: Discussionmentioning

confidence: 99%

“…For example, Solyc11g011080, which is enhanced in Red Setter and Moneymaker at 25 • C codes for a putative disease resistance protein, while Solyc11g018800 which is higher expressed in Red Setter and Moneymaker at 39 • C codes for a peroxidase LePrx26 involved in pathogen response [55]. However, most of the genes of this category are found to be differentially regulated at 45 • C. For instance, a putative glutaredoxin (Solyc06g008760) is downregulated in Red Setter at 45 • C. Glutaredoxins are important for redox regulation, which is essential for thermotolerance, and it has been previously shown that overexpression of an A. thaliana glutaredoxin enhances both drought and HS tolerance in tomato [56,57]. In contrast, Solyc01g081250, Solyc09g005420 and Solyc11g011010 are upregulated at 45 • C in Red Setter when compared to the other genotypes.…”

Section: Genotype-specific Transcriptome Responses To Elevated Tempermentioning

confidence: 99%

Transcriptional Basis for Differential Thermosensitivity of Seedlings of Various Tomato Genotypes

Fragkostefanakis

Schleiff

et al. 2020

Genes

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Transcriptional reprograming after the exposure of plants to elevated temperatures is a hallmark of stress response which is required for the manifestation of thermotolerance. Central transcription factors regulate the stress survival and recovery mechanisms and many of the core responses controlled by these factors are well described. In turn, pathways and specific genes contributing to variations in the thermotolerance capacity even among closely related plant genotypes are not well defined. A seedling-based assay was developed to directly compare the growth and transcriptome response to heat stress in four tomato genotypes with contrasting thermotolerance. The conserved and the genotype-specific alterations of mRNA abundance in response to heat stress were monitored after exposure to three different temperatures. The transcripts of the majority of genes behave similarly in all genotypes, including the majority of heat stress transcription factors and heat shock proteins, but also genes involved in photosynthesis and mitochondrial ATP production. In turn, genes involved in hormone and RNA-based regulation, such as auxin- and ethylene-related genes, or transcription factors like HsfA6b, show a differential regulation that associates with the thermotolerance pattern. Our results provide an inventory of genes likely involved in core and genotype-dependent heat stress response mechanisms with putative role in thermotolerance in tomato seedlings.

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“…GRXS17 was previously proposed to improve thermo-, drought- and oxidative-tolerance by enhancing ROS scavenging capacities and expression of Heat-Shock Proteins. This might occur by modulation of gene expression, enzyme activity or protection of antioxidant enzymes (Wu et al, 2012, 2017; Hu et al, 2017). Our data suggest an additional function of GRXS17 through its chaperone activity.…”

Section: Discussionmentioning

confidence: 99%

“…However, for most of its partners, the role of the Fe-S cluster remained enigmatic. Genetic evidence from different plant species suggests a protective role of GRXS17 during thermal, genotoxic and drought stress (Cheng et al, 2011; Wu et al, 2012; Wu et al, 2017; Iñigo et al, 2016; Hu et al, 2017), in meristem development (Knuesting et al, 2015), hormonal responses (Cheng et al, 2011), and during redox-dependent processes (Yu et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Redox response of iron-sulfur glutaredoxin GRXS17 activates its holdase activity to protect plants from heat stress

Martins

Knuesting

Bariat

et al. 2020

Preprint

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Living organisms use a large panel of mechanisms to protect themselves from environmental stress.Particularly, heat stress induces misfolding and aggregation of proteins which are guarded by chaperone systems. Here, we examine the function the glutaredoxin GRXS17, a member of thiol reductases families in the model plant Arabidopsis thaliana. GRXS17 is a nucleocytosolic 30 monothiol glutaredoxin consisting of an N-terminal thioredoxin (TRX)-domain and three CGFSactive site motif-containing GRX-domains that coordinate three iron-sulfur (Fe-S) clusters in a glutathione (GSH)-dependent manner. As a Fe-S cluster-charged holoenzyme, GRXS17 is likely involved in the maturation of cytosolic and nuclear Fe-S proteins. In addition to its role in cluster biogenesis, we showed that GRXS17 presents both foldase and redox-dependent holdase activities. 35Oxidative stress in combination with heat stress induces loss of its Fe-S clusters followed by subsequent formation of disulfide bonds between conserved active site cysteines in the corresponding TRX domains. This oxidation leads to a shift of GRXS17 to a high-MW complex and thus, activates its holdase activity. Moreover, we demonstrate that GRXS17 is specifically involved in plant tolerance to moderate high temperature and protects root meristematic cells from 40 heat-induced cell death. Finally, we showed that upon heat stress, GRXS17 changes its client proteins, possibly to protect them from heat injuries. Therefore, we propose that the iron-sulfur cluster enzyme glutaredoxin GRXS17 is an essential guard to protect proteins against moderate heat stress, likely through a redox-dependent chaperone activity. All in all, we reveal the mechanism of an Fe-S cluster-dependent activity shift, turning the holoenzyme GRXS17 into a holdase that 45 prevents damage caused by heat stress.

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Expression of a monothiol glutaredoxin, AtGRXS17, in tomato (Solanum lycopersicum) enhances drought tolerance

Cited by 42 publications

References 45 publications

CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance

CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance

Transcriptional Basis for Differential Thermosensitivity of Seedlings of Various Tomato Genotypes

Redox response of iron-sulfur glutaredoxin GRXS17 activates its holdase activity to protect plants from heat stress

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