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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: 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.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.

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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Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione reductases in susceptible plants, but not in resistant plants.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione reductases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AY364467. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to FK827496.
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f4: Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione reductases in susceptible plants, but not in resistant plants.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione reductases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AY364467. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to FK827496.

Mentions: Glutathione reductases convert GSSG back into GSH using NADPH as an electron donor so that GSH can be reused for detoxification. Enzymatic activity of glutathione reductases increased steadily in susceptible plants after Hessian fly infestation (Figure 4a). However, no significant change was observed in the level of glutathione reductase activity in infested 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 reductases in susceptible plants, but not in resistant plants.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione reductases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AY364467. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to FK827496.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Hessian fly induces higher levels of enzymatic activity and transcript abundance of glutathione reductases in susceptible plants, but not in resistant plants.Black and grey bars represent data from susceptible (Newton) and resistant (Molly) plants, respectively. (a) Percentage change in enzymatic activity of glutathione reductases in plants at different time points after Hessian fly infestation. (b) Fold changes of transcript abundance determined by qPCR using the primer pair specific to AY364467. (c) Fold changes of transcript abundance determined by qPCR using the primer pair specific to FK827496.
Mentions: Glutathione reductases convert GSSG back into GSH using NADPH as an electron donor so that GSH can be reused for detoxification. Enzymatic activity of glutathione reductases increased steadily in susceptible plants after Hessian fly infestation (Figure 4a). However, no significant change was observed in the level of glutathione reductase activity in infested resistant plants.

Bottom Line: 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.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.

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