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Unbalanced activation of glutathione metabolic pathways suggests potential involvement in plant defense against the gall midge Mayetiola destructor in wheat.

Liu X, Zhang S, Whitworth RJ, Stuart JJ, Chen MS - Sci Rep (2015)

Bottom Line: However, the enzymatic activity and transcript abundance of glutathione reductases, which convert GSSG back to GSH, did not change.Our data suggest the possibility that GSSG is transported from cytosol to apoplast to serve as an oxidant for class III peroxidases to generate reactive oxygen species for plant defense against Hessian fly larvae.Our results provide a foundation for elucidating the molecular processes involved in glutathione-mediated plant resistance to Hessian fly and potentially other pests as well.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506.

ABSTRACT
Glutathione, γ-glutamylcysteinylglycine, exists abundantly in nearly all organisms. Glutathione participates in various physiological processes involved in redox reactions by serving as an electron donor/acceptor. We found that the abundance of total glutathione increased up to 60% in resistant wheat plants within 72 hours following attack by the gall midge Mayetiola destructor, the Hessian fly. The increase in total glutathione abundance, however, is coupled with an unbalanced activation of glutathione metabolic pathways. The activity and transcript abundance of glutathione peroxidases, which convert reduced glutathione (GSH) to oxidized glutathione (GSSG), increased in infested resistant plants. However, the enzymatic activity and transcript abundance of glutathione reductases, which convert GSSG back to GSH, did not change. This unbalanced regulation of the glutathione oxidation/reduction cycle indicates the existence of an alternative pathway to regenerate GSH from GSSG to maintain a stable GSSG/GSH ratio. Our data suggest the possibility that GSSG is transported from cytosol to apoplast to serve as an oxidant for class III peroxidases to generate reactive oxygen species for plant defense against Hessian fly larvae. Our results provide a foundation for elucidating the molecular processes involved in glutathione-mediated plant resistance to Hessian fly and potentially other pests as well.

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Related in: MedlinePlus

Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione synthetases.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione synthetases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair common to CK156077, AJ579381 and AJ579382. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AJ579380.
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f2: Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione synthetases.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione synthetases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair common to CK156077, AJ579381 and AJ579382. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AJ579380.

Mentions: To determine if the increase in glutathione abundance is due to increased synthesis, we determined the activity of γ-glutamylcysteine synthetase and glutathione synthetase in wheat tissue at the feeding site. The enzymatic activities of these two enzymes were differentially regulated. The enzymatic activity of γ-glutamylcysteine synthetase did not change significantly in infested resistant plants (Figure S2). Consistent with the finding that there is no apparent increase in enzymatic activity, the transcript levels of genes encoding γ-glutamylcysteine synthetases did not change significantly either. On the other hand, the enzymatic activity of glutathione synthetase increased steadily in wheat tissue at the feeding site in resistant plants starting from three hours after Hessian fly infestation (Figure 2a). The increase in glutathione synthetase activity reached a maximum at 48 hours, and started to decrease at 72 hours after Hessian fly infestation. In susceptible plants, the enzymatic activity of glutathione synthetase decreased slightly in wheat tissue at the feeding site at three and 12 hours following Hessian fly infestation. At 24, 48, and 72 hours, glutathione synthetase activity increased in susceptible plants, but the increase was of a much smaller magnitude in comparison with that observed in resistant plants.


Unbalanced activation of glutathione metabolic pathways suggests potential involvement in plant defense against the gall midge Mayetiola destructor in wheat.

Liu X, Zhang S, Whitworth RJ, Stuart JJ, Chen MS - Sci Rep (2015)

Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione synthetases.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione synthetases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair common to CK156077, AJ579381 and AJ579382. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AJ579380.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4308708&req=5

f2: Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione synthetases.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione synthetases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair common to CK156077, AJ579381 and AJ579382. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AJ579380.
Mentions: To determine if the increase in glutathione abundance is due to increased synthesis, we determined the activity of γ-glutamylcysteine synthetase and glutathione synthetase in wheat tissue at the feeding site. The enzymatic activities of these two enzymes were differentially regulated. The enzymatic activity of γ-glutamylcysteine synthetase did not change significantly in infested resistant plants (Figure S2). Consistent with the finding that there is no apparent increase in enzymatic activity, the transcript levels of genes encoding γ-glutamylcysteine synthetases did not change significantly either. On the other hand, the enzymatic activity of glutathione synthetase increased steadily in wheat tissue at the feeding site in resistant plants starting from three hours after Hessian fly infestation (Figure 2a). The increase in glutathione synthetase activity reached a maximum at 48 hours, and started to decrease at 72 hours after Hessian fly infestation. In susceptible plants, the enzymatic activity of glutathione synthetase decreased slightly in wheat tissue at the feeding site at three and 12 hours following Hessian fly infestation. At 24, 48, and 72 hours, glutathione synthetase activity increased in susceptible plants, but the increase was of a much smaller magnitude in comparison with that observed in resistant plants.

Bottom Line: However, the enzymatic activity and transcript abundance of glutathione reductases, which convert GSSG back to GSH, did not change.Our data suggest the possibility that GSSG is transported from cytosol to apoplast to serve as an oxidant for class III peroxidases to generate reactive oxygen species for plant defense against Hessian fly larvae.Our results provide a foundation for elucidating the molecular processes involved in glutathione-mediated plant resistance to Hessian fly and potentially other pests as well.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506.

ABSTRACT
Glutathione, γ-glutamylcysteinylglycine, exists abundantly in nearly all organisms. Glutathione participates in various physiological processes involved in redox reactions by serving as an electron donor/acceptor. We found that the abundance of total glutathione increased up to 60% in resistant wheat plants within 72 hours following attack by the gall midge Mayetiola destructor, the Hessian fly. The increase in total glutathione abundance, however, is coupled with an unbalanced activation of glutathione metabolic pathways. The activity and transcript abundance of glutathione peroxidases, which convert reduced glutathione (GSH) to oxidized glutathione (GSSG), increased in infested resistant plants. However, the enzymatic activity and transcript abundance of glutathione reductases, which convert GSSG back to GSH, did not change. This unbalanced regulation of the glutathione oxidation/reduction cycle indicates the existence of an alternative pathway to regenerate GSH from GSSG to maintain a stable GSSG/GSH ratio. Our data suggest the possibility that GSSG is transported from cytosol to apoplast to serve as an oxidant for class III peroxidases to generate reactive oxygen species for plant defense against Hessian fly larvae. Our results provide a foundation for elucidating the molecular processes involved in glutathione-mediated plant resistance to Hessian fly and potentially other pests as well.

Show MeSH
Related in: MedlinePlus