Recovery of photosynthesis, sucrose metabolism, and proteolytic enzymes in Kandelia obovata from rare cold events in the northernmost mangrove, China

Zheng et al. Ecological Processes Recovery of photosynthesis, sucrose metabolism, and proteolytic enzymes in Kandelia obovata from rare cold events in the northernmost mangrove, China Chunfang Zheng 1 Yong Ye Weicheng Liu 1 Jianwu Tang 0 Chengnian Zhang Jianbiao Qiu 1 Jinong Chen 1 0 Nanji Islands National Marine Nature Reserve Administration , Pingyang , China 1 Wenzhou Ocean Research Institute, Zhejiang Key Laboratory of Exploitation and Preservation of Coastal Bio-resource, Zhejiang Mariculture Research Institute , Wenzhou 325000 , China Introduction: Understanding how mangroves respond to rare cold events has implications for both restoration and conservation under climate change scenarios. This study investigated the responses of photosynthesis and activities of key enzymes involving carbon and nitrogen metabolism at different ages of Kandelia obovata to a rare cold event in the winter of 2010. Methods: This study took place on Ximen Island, Zhejiang Province, China. We measured the physiological recovery of 2-3-, 5-6-, 9-10- and 54-55-year-old K. obovata trees after freezing injury in February and March in 2011 and 2012, respectively. Results: Chilling injury index and electrolyte leakage of K. obovata increased with increasing tree age in the winter of 2010, and electrolyte leakage in K. obovata at different ages in the winter of 2010 was far higher than that in the winter of 2011. The rare cold events significantly changed the recoveries of the leaf net photosynthetic rate (Pn) and stomatal conductance (Gs); ratios of chlorophyll a/chlorophyll b (Chl a/Chl b); contents of total soluble sugar (TSS), sucrose, free amino acid (FAA), and soluble protein; and activities of sucrose phosphate synthase (SPS), endopeptidase, and carboxypeptidase in K. obovata at different ages. These effects were mainly due to changes in the physiological mechanism in the 2-year-old trees. A clear decrease in Pn of the 2-year-old trees was observed in February 2011, as exemplified by reductions in ratios of Chl a/Chl b and chlorophyll/carotenoid (Chl/Car), as well as inhibition of the levels of TSS and FAA (osmotic substances). During recovery in 2011 and 2012, the activities of SPS and sucrose synthase (SS) were responsible for sucrose synthesis after the rare cold events in 2011, but only SPS activity was one of the main factors contributing to the metabolism of stachyose to sucrose without cold damage in 2012. Carboxypeptidase played a more important role than endopeptidase during protein hydrolysis after the rare cold events. Conclusions: The results suggest that the recovery of photosynthetic capacity in K. obovata was changed after a rare cold event, which is associated with pigment components and activities of SS, SPS, and carboxypeptidase, especially the seedlings. Kandelia obovata; Photosynthesis; Sucrose synthase; Rare cold events; Peptidase Introduction Mangroves are open ecosystems that straddle the land and the sea, from freshwater to seawater, providing diverse habitats for plant and animal species (Li and Less 1997) . They are one of the most productive ecosystems in the world and provide a variety of ecological and societal goods and services (Liu et al. 2014) , such as nursing fishes (Levy et al. 2015) , maintaining biodiversity (Thornton and Johnstone 2015) , and absorbing pollution (Debenay et al. 2015) . Despite their ecological relevance, mangroves that grow along the latitudinal extremes of their distribution in subtropical and tropical environments are extremely vulnerable to low temperature (Ellis et al. 2006) . Low temperature can seriously affect the growth, development, nutrient resorption, and survival of mangroves in coastal tidal wetlands (McMillam 1971; Wang et al. 2011b) . Global warming can result in mangrove forests migrating to higher latitudes, either naturally or with human-assisted migration (Field 1995; Gilman et al. 2008) . However, extreme cold events may slow down this migration. For example, frost damage that occurred in 2008 resulted in the death of a significant number of mangrove seedlings introduced into the southeast coast of China and early drop of flowers and fruits of mature trees, thereby damaging the natural regeneration and reforestation of mangroves in the forthcoming 1 or 2 years (Chen et al. 2010). Thus, current physiological and ecological studies are focusing on the cold damage of mangroves. Kao et al. (2004) demonstrated that the leaves of Kandelia obovata Sheue, Liu & Yong (2003) show a reduction in light-saturated photosynthetic rates, stomatal conductance, electron transport rates, and quantum yields of photosystem II after exposure to 15 °C for 1 h. In recent years, combined with continuing research on cold damage in mangroves, the recovery of physiological and ecological functions of mangroves after low temperature stress has attracted increasing attention. Studies on the recovery from low temperatures mainly focused on extreme temperatu (...truncated)