Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants

The Chinese hickory (Carya cathayensis) is an economically important tree species popular for its nuts. However, the tree requires a long time to reach the nut-producing phase. To overcome this problem, grafting is widely used to reduce the time from the vegetative to the reproductive phase. This tree species also faces many environmental challenges due to climate change; drought is an important factor affecting growth and development. Here, we designed an experiment to assess the protective efficiency of melatonin in grafted Chinese hickory plants under drought stress. The results revealed that exogenously applied melatonin successfully recovered the growth of grafted Chinese hickory plants and improved photosynthetic efficiency. Exogenously applied melatonin also boosted the antioxidative defense system of the plants under drought stress, resulting in enhanced reactive oxygen species (ROS) scavenging. The accumulation of compatible solutes such as total soluble sugars and proline was also triggered by melatonin. Moreover, the analyses using metabolomics revealed that drought-stressed plants treated with melatonin regulated key metabolic pathways such as phenylpropanoid, chlorophyll and carotenoid biosynthesis, carbon fixation, and sugar metabolism. To further validate the physiological, biochemical, and metabolomic factors, we studied the molecular mechanisms by analyzing the expression of key genes involved in chlorophyll metabolism (chlorophyllase, CHLASE), antioxidative defense (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; peroxidase, POD), and phenylalanine ammonia-lyase (PAL). Exogenously applied melatonin significantly regulated the transcript levels of key genes involved in the biological processes mentioned above. Melatonin also showed crosstalk with other hormones (zeatin, gibberellin A14, 24-epibrassinolide, jasmonic acid, and abscisic acid) to regulate the physiological processes. The results of this study show that melatonin regulates biological processes at the metabolic and molecular levels to resist drought stress.