Role of Glutathione-Ascorbate Cycle and Photosynthetic Electronic Transfer in Alternative Oxidase-Manipulated Waterlogging Tolerance in Watermelon Seedlings

Alternative oxidase (AOX) has been documented to mitigate the oxidative stress caused by abiotic stresses. However, it remains unknown how AOX regulates the antioxidant system and photosynthesis under waterlogging. To address this issue, we used two watermelon (Citrullus lanatus L.) cultivars (waterlogging tolerant cultivar 'YL' and sensitive cultivar 'Zaojia8424') as materials and the AOX inhibitor salicylhydroxamic acid (SHAM) to investigate the effects of AOX on photosynthesis and reactive oxygen species metabolism under waterlogging. We found that waterlogging decreased leaf photosynthesis and quantum yield of photosynthesis in watermelon, and the waterlogging tolerant cultivar 'YL' showed higher expression level of ClaAOX than the sensitive cultivar 'Zaojia8424'. Net photosynthesis rate was higher in 'YL' than 'Zaojia8424'. Moreover, waterlogging induced photoinhibition in 'Zaojia8424' but not in 'YL'. Meanwhile, waterlogging promoted the accumulation of superoxide and peroxide hydrogen, and triggered oxidative damage. 'YL' suffered from less severe oxidative damage due to increased contents of ascorbate, a higher ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG), a higher activity of ascorbate peroxidase (APX) and catalase (CAT), and enhanced levels of CAT and APX expression, relative to 'Zaojia8424'. However, the alleviation of photosynthesis and oxidative damage, increased content of ascorbate and higher GSH/GSSG ratio were abolished by SHAM. Our results suggested that photosynthetic electronic transfer and glutathione-ascorbate cycle are involved in waterlogging tolerance mediated by the AOX pathway in watermelon.

Automated summary

The study revealed that under waterlogging conditions, watermelon cultivar 'YL' exhibited higher expression of ClaAOX, which led to better photosynthesis and less oxidative damage compared to watermelon cultivar 'Zaojia8424'. Additionally, the alleviation of oxidative damage and promotion of photosynthesis in 'YL' were associated with increased levels of ascorbate, higher GSH/GSSG ratio, and enhanced activity of antioxidant enzymes, such as APX and CAT.