Melatonin enhances waterlogging tolerance of field-grown cotton through quiescence adaptation and compensatory growth strategies

Context: Waterlogging stress inhibits plant growth and development, resulting in significant yield losses. Melatonin, a naturally occurring molecule in plants, has attracted attention in recent years for its potential role in aiding plants in response to abiotic stresses. However, it remains unclear whether melatonin can enhance cotton's tolerance to waterlogging stress. Methods: To fill this gap, field-grown cotton plants at early flowering were subjected to a 10-day waterlogging stress and were foliar sprayed with melatonin during waterlogging. The effects of melatonin on the endogenous melatonin concentration, plant biomass, and related physiological and molecular events, as well as the seedcotton yield and yield components, were evaluated over two consecutive years. Results: In waterlogged cotton without melatonin treatment (W), melatonin concentration increased by 10.2%, but it increased by 26.9% with melatonin treatment (W+M), compared to the non-waterlogged cotton (NW). Under waterlogging without the application of melatonin, there was a reduction of 27.1% in biological yield and 46.6% in seedcotton yield. However, these reductions were reduced to 21.8% and 39.0%, respectively, following melatonin application. Quantitative real-time PCR analysis revealed that melatonin up-regulated the melatonin biosynthesis genes GhSNAT1 and GhCOMT, as well as the gibberellin biosynthetic gene GhGA20ox1 by 2.1, 3.6 and 1.8 times, respectively, compared to non-waterlogged cotton. However, melatonin down-regulated the ABA synthesis gene GhNCED2, the H2O2 generation related gene GhRBOHC, and the glycolysis and fermentation gene GhADH2 by 61.9%, 65.0% and 40.0%, respectively. Additionally, melatonin increased the leaf chlorophyll content, photosynthetic rate, levels of auxin (IAA) and gibberellic acid (GA), as well as the activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT). Conversely, melatonin reduced contents of hydrogen peroxide (H2O2), malonaldehyde (MDA) and ABA, as well as the activities of alcohol dehydrogenase (ADH) and pyruvate decarboxylase (PDC), compared to waterlogging without application of melatonin. Conclusions: These findings demonstrate that foliar application of melatonin effectively improved the waterlogging tolerance of field-grown cotton, leading to a reduction in yield loss by 16.5% under waterlogged conditions. This outcome was achieved by a series of physiological, biological and molecular adjustments involved in quiescence adaption and compensatory growth strategies. Therefore, melatonin plays a crucial role in enhancing waterlogging tolerance and mitigating yield loss in waterlogged cotton through these strategies.