Hydrogen sulfide upregulates the alternative respiratory pathway in mangrove plant Avicennia marina to attenuate waterlogging‐induced oxidative stress and mitochondrial damage in a calcium‐dependent manner.

Hydrogen sulfide (H2S) is considered to mediate plant growth and development. However, whether H2S regulates the adaptation of mangrove plant to intertidal flooding habitats is not well understood. In this study, sodium hydrosulfide (NaHS) was used as an H2S donor to investigate the effect of H2S on the responses of mangrove plant Avicennia marina to waterlogging. The results showed that 24‐h waterlogging increased reactive oxygen species (ROS) and cell death in roots. Excessive mitochondrial ROS accumulation is highly oxidative and leads to mitochondrial structural and functional damage. However, the application of NaHS counteracted the oxidative damage caused by waterlogging. The mitochondrial ROS production was reduced by H2S through increasing the expressions of the alternative oxidase genes and increasing the proportion of alternative respiratory pathway in the total mitochondrial respiration. Secondly, H2S enhanced the capacity of the antioxidant system. Meanwhile, H2S induced Ca2+ influx and activated the expression of intracellular Ca2+‐sensing‐related genes. In addition, the alleviating effect of H2S on waterlogging can be reversed by Ca2+ chelator and Ca2+ channel blockers. In conclusion, this study provides the first evidence to explain the role of H2S in waterlogging adaptation in mangrove plants from the mitochondrial aspect. Summary statement: H2S reduces mitochondrial ROS production by increasing the expressions of the alternative oxidase gene (AOX) and increases the proportion of alternative respiratory pathway in the total respiration, while H2S alleviates the mitochondrial structural damages including loss of bilayer membranes and blurring of mitochondrial cristae, and functional damages such as decrease of mitochondrial membrane potential (ΔΨm), membrane permeability transition pores opening, Cyt c release and the blockage of electron transfer along the mitochondrial electron transport chain caused by waterlogging‐induced oxidative stress. Secondly, H2S enhances the capacity of the antioxidant system through upregulating the expression of SOD, CAT, and APX genes to scavenge excess ROS. Last, H2S induces Ca2+ influx in the roots under waterlogging. Our results provide the better understanding of the role of H2S in adaptation of mangrove plants to the coastal intertidal environment from the mitochondrial aspect. [ABSTRACT FROM AUTHOR]