Abstract
Cellular redox homeostasis is essential for plant growth, development as well as for the resistance to biotic and abiotic stresses, which is governed by the complex network of prooxidant and antioxidant systems. Recently, new evidence has been published that NADPH, produced by glucose-6-phosephate dehydrogenase enzyme (G6PDH), not only acted as the reducing potential for the output of reduced glutathione (GSH), but was involved in the activity of plasma membrane (PM) NADPH oxidase under salt stress, which resulted in hydrogen peroxide (H2O2) accumulation. H2O2 acts as a signal in regulating G6PDH activity and expression, and the activities of the enzymes in the glutathione cycle as well, through which the ability of GSH regeneration was increased under salt stress. Thus, G6PDH plays a critical role in maintaining cellular GSH levels under long-term salt stress. In this addendum, a hypothetical model for the roles of G6PDH in modulating the intracellular redox homeostasis under salt stress is presented.
Key words: glucose-6-phosphate dehydrogenase, hydrogen peroxide, reduced glutathione, redox homeostasis, salt stress
Environmental stresses inevitably induce the production of reactive oxygen species (ROS).1 Reduced glutathione (GSH) is a key substance in the network of antioxidants that include ascorbate, glutathione, α-tocopherol and a serial of antioxidant enzymes,2 which metabolizes H2O2 mainly via the ascorbate-glutathione cycle, the most important detoxifying system in plants.3 Thus, the regulatory ability to maintain the cellular GSH balance is crucial to confer the resistance to oxidative stress in plants. However, to our knowledge, the regulatory mechanism on the intracellular GSH-pool equilibrium under environmental stresses has been largely unknown in plants.
A main source of GSH is regenerated from its oxidative form (GSSG) via glutathione cycling, which uses NADPH as the reductant.4 G6PDH is the key enzyme of pentose phosphate pathway that is responsible for the generation of NADPH.5 G6PDH has been shown to play a protective role against ROS in human and animal cells,6,7 and the enhanced expression of G6PDH could enhance the GSH levels and the ability of resistance to oxidative stress.5,8 In plants, it has been reported that oxidative stress induced by the elicitor stimulated G6PDH activity in tobacco cells,9,10 and the GSH-biosynthesis inhibitor or GSH precursor could increase or suppressed G6PDH activity, respectively.10 Interestingly, after G6PDH activity was inhibited, not only GSH levels dramatically decreased, but the elicitor-induced H2O2 accumulation was also completely counteracted.9,10 Thus, the functions of G6PDH under oxidative stress seem to be involved in these two contradictory courses in cells: the regeneration of GSH as well as H2O2 accumulation. The role of G6PDH under environmental stresses remained limited to clarify this, so we studied the G6PDH functions with a series of inhibitor or donor of GSH, H2O2 and G6PDH in reed calli under salt stress. Our recent studied clearly demonstrated that G6PDH activity was also simultaneously involved in intracellular GSH maintenance and H2O2 accumulation in salt stress. Further studies revealed that a plasma membrane (PM) NADPH oxidase, using NADPH as substrate mainly produced by G6PDH, was mainly responsible for the generation of H2O2. And H2O2, produced under salt stress, induced the increased G6PDH activity and the enzymes of glutathione cycle, which concomitantly resulted in an increased GSH contents. Foyer and Noctor (2005) suggested that the cellular “oxidative signaling” was made possibly by homeostatic regulation by antioxidant redox buffer.11 Based on these, it can be speculated that G6PDH might play an important role in maintaining the cellular redox signals under salt stress in plants.
Our recent work provides a new insight into G6PDH functions under environmental stresses in plants. Growing evidences suggest that PM NADPH oxidase is responsible for H2O2 accumulation under stresses,12,13 and H2O2 is involved in various signaling pathways in plants, such as defense gene expression, stomatal closure, root growth, programmed cell death (PCD) and so on.11 In addition, GSH, as a key antioxidant, also influences gene expression associated with biotic and abiotic stress responses to maximum defense.2 Recent study also reported that G6PDH was involved in NR-dependent NO production, and thus played a pivotal role in establishing tolerance of red kidney bean roots to salt stress.14 Therefore, the research work is required to further clarify the regulatory mechanism underlying the roles of G6PDH in the cellular redox homeostasis as well as the related signals under environmental stresses in plants.
Based on the results obtained so far, a model for G6PDH functions under salt stress is proposed (Fig. 1). In our model, the increased G6PDH activity is tightly correlated with GSH maintenance and H2O2 accumulation through PM NADPH oxidase under salt stress in plants. Under salt stress, H2O2 activities the activities of G6PDH and the enzymes in glutathione recycle, which finally result in the enhanced glutathione cycling rate and thus the increased GSH levels. This enhanced antioxidant ability can facilitate to maintain a steady-state level of H2O2. Eventually, the properly intracellular redox state is established under salt stress and forms a metabolic interface for signals. Thus, we suggest that G6PDH plays a crucial role in establishing this cellular redox homeostasis under salt stress.
Figure 1.
Hypothetical model for the roles of G6PDH under salt stress. Under salt stress, G6PDH activity is involved in both GSH maintenance and H2O2 accumulation through PM NADPH oxidase. H2O2, as a signal, increases the activities of G6PDH, glutathione (GR) and glutathione peroxidase (GPX), which finally enhance glutathione cycle rate and result in the increased GSH levels. This enhanced antioxidant ability could facilitate to keep H2O2 in a steady state for signal in salt stress.
Acknowledgements
This work was supported by Specialized Research Fund for the Doctoral Program of Higher Education of China (ratification number: 20050730017), Foundation of Science and Technology of Gansu Province (3ZS051-A25-01).
Footnotes
Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/5372
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