Key photoprotective pathways of a shade-tolerant plant (Alpinia oxyphylla) for precipitation patterns change during the dry season: thermal energy dissipation and water-water cycle

Abstract

Alpinia oxyphylla Miq is a shade-tolerant plant that grows under rubber trees. The decreased precipitation often leads to limitation of photosynthesis and productivity of A. oxyphylla during the dry season. However, the effects of the precipitation patterns on the photosynthesis and the photoprotective strategies of A. oxyphylla remains unclear. Herein, we examined how CO2 assimilation, light energy partitioning and reactive oxygen species (ROS) metabolism are affected by simulated precipitation patterns change. The change of precipitation patterns induced water deficits of different intensities and durations. With the decreased precipitation, stomatal conductance (Gs) and net CO2 assimilation rate (Pn) significantly decreased, resulting in excess excitation energy and over-accumulation of ROS, and further caused lipid peroxidation of photosynthetic apparatus. The phenomenon was exacerbated by extending the interval between precipitation. In addition, the decreased precipitation induced the xanthophyll cycle effectively dissipating excess excitation energy. Through the water-water cycle, a greater proportion of electron flux was shuffled to molecular oxygen (O2) to produce superoxide anion (O2•−), especially in plants under natural precipitation (W; 25 mm/month). This may be because the energy partitioning mechanism of A. oxyphylla can efficiently dissipate excessive excitation energy and reduce PSⅡ photoinhibition, thus rapidly adapting to precipitation patterns change. On the other hand, the decreased precipitation improved the capacity of ROS detoxification in the water-water cycle and reduced lipid peroxidation in W plants, which were reflected by the increase of SOD and CAT activities, and a partial enhancement of antioxidant enzymes and antioxidant metabolism in the water-water cycle. However, the down-regulation of antioxidant systems in W- plants (decreased precipitation; 10 mm/month) further accelerated ROS accumulation and the ability of ROS-scavenging might be partially compensated by ROS accumulation, which may had been a primary cause for limited the antioxidant protection. Overall, when CO2 assimilation reduced with the decreased precipitation, A. oxyphylla can form a photoprotective mechanism, both thermal energy dissipation and water-water cycle are crucial photoprotective pathways against photodamage in photosynthetic apparatus.