Abstract
The viability of recalcitrant seeds is lost following stress from either drying or freezing. Reactive oxygen species (ROS) resulting from uncontrolled metabolic activity are likely responsible for seed sensitivity to drying. Nitric oxide (NO) and the ascorbate-glutathione cycle can be used for the detoxification of ROS, but their roles in the seed response to desiccation remain poorly understood. Here, we report that desiccation induces rapid accumulation of H2O2, which blocks recalcitrant Antiaris toxicaria seed germination; however, pretreatment with NO increases the activity of antioxidant ascorbate-glutathione pathway enzymes and metabolites, diminishes H2O2 production and assuages the inhibitory effects of desiccation on seed germination. Desiccation increases the protein carbonylation levels and reduces protein S-nitrosylation of these antioxidant enzymes; these effects can be reversed with NO treatment. Antioxidant protein S-nitrosylation levels can be further increased by the application of S-nitrosoglutathione reductase inhibitors, which further enhances NO-induced seed germination rates after desiccation and reduces desiccation-induced H2O2 accumulation. These findings suggest that NO reinforces recalcitrant seed desiccation tolerance by regulating antioxidant enzyme activities to stabilize H2O2 accumulation at an appropriate concentration. During this process, protein carbonylation and S-nitrosylation patterns are used as a specific molecular switch to control antioxidant enzyme activities.
Highlights
Recalcitrant seeds, known as unorthodox seeds, lose viability following exposure to either drying or freezing conditions after being shed from the parent plant
During the course of desiccation by air-drying, the germination capability declined with the loss of water, and the decline was accompanied by increasing electrolyte leakage, which result in membrane disintegration
A strong correlation was found among seed viability determinants such as seed germination and H2O2 and Nitric oxide (NO) levels after three days of desiccation (Table S1), which indicates that both H2O2 and NO are involved in the mechanism of seed intolerance to desiccation
Summary
Recalcitrant seeds, known as unorthodox seeds, lose viability following exposure to either drying or freezing conditions after being shed from the parent plant. The glutathione-ascorbate cycle is a metabolic pathway that can efficiently detoxify H2O2. This pathway involves antioxidant metabolites including ascorbate, glutathione and NADPH, and the enzymes linking these metabolites pathway include ascorbate peroxide (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDAR) and dehydroascorbate reductase (DHAR). In the first step of this pathway, H2O2 is reduced to water by APX using ascorbate as the electron donor. The oxidized ascorbate (monodehydroascorbate or dehydroascorbate) is regenerated by MDAR and DHAR at the expense of reduced glutathione (GSH), yielding oxidized glutathione (GSSG). Glutathione, ascorbate and NADPH are present in high concentrations; it is assumed that the glutathione-ascorbate cycle plays a key role in H2O2 detoxification [4]
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