Drought tolerance in wheat: role of TaCOMT1A in melatonin and sakuranetin contents

Drought stress significantly affects global food security, particularly in arid and semi-arid farming regions. Wheat (Triticum aestivum L.), one of the most critical staple crops worldwide, experiences substantial growth and yield losses under drought conditions. Caffeic acid O-methyltransferase (COMT) is a key enzyme in the phenylpropanoid metabolic pathway, playing a pivotal role in the biosynthesis of flavonoids, lignin, and melatonin, among other metabolites. Melatonin, a multifunctional signaling molecule, promotes plant growth and mitigates biotic and abiotic stresses, including drought, cold, and salinity. Sakuranetin, a methoxylated flavonoid functioning as a phytoalexin, is induced by environmental stimuli such as jasmonic acid (JA), UV light, and pathogen invasions. However, the role of COMT in wheat (TaCOMT1A) and the mechanisms by which melatonin and sakuranetin regulate drought tolerance remain poorly understood. This study systematically examines the multifunctionality of COMT and sakuranetin in plants and highlights recent advances in melatonin-mediated drought tolerance. To address key gaps, we designed three research directions:
(1) Overexpression of TaCOMT1A enhances drought tolerance in wheat. Transgenic wheat lines overexpressing TaCOMT1A exhibited enhanced drought tolerance during both seedling and maturation stages compared to wild-type (WT) plants. Under field drought conditions, these lines achieved a 15.21%–20.27% increase in grain weight per plant while exhibiting a 10.92%–12.47% reduction in plant height compared to WT. Metabolomic analysis revealed elevated levels of key flavonoids, including sakuranetin, isorhamnetin, vitexin, kaempferol, and narcissin in the overexpression lines. Biochemical studies showed that TaCOMT1A directly synthesizes sakuranetin and melatonin, underscoring its multifunctional enzymatic activity in drought tolerance.
(2) Melatonin enhances wheat drought tolerance. Exogenous application of melatonin (100 μM) significantly improved drought tolerance in wheat varieties such as “Chinese Spring,” “Shi4185,” and “Hanxuan10,” but not “Chang6878.” Transcriptomic and proteomic analyses demonstrated that melatonin enhances JA biosynthesis by upregulating LOX1.5, LOX2.1, and transcription factors HY5 and MYB86. It also increased lignin biosynthesis (4CL2, P5CS1, CCR2) and starch metabolism (PME53, SUS4), while mitigating oxidative damage by maintaining low hydrogen peroxide levels. These findings suggest that melatonin enhances drought resilience by upregulating JA and lignin biosynthesis and offers a potential eco-friendly biostimulant for improving wheat productivity.
(3) Sakuranetin reduces plant height and improves drought tolerance. Exogenous application of sakuranetin also conferred drought tolerance and reduced plant height in conventional wheat varieties. Transcriptomic analysis indicated that sakuranetin alleviates drought stress by upregulating photosynthesis-related genes and downregulating gibberellic acid (GA) biosynthesis genes, such as TaGA2ox-5B and TaKO-7A. Additionally, sakuranetin enhanced drought tolerance by upregulating the key drought-responsive gene TaDREB2C-1A. These results highlight sakuranetin as a promising candidate for improving drought tolerance and regulating plant height.
Overall, this study elucidates the role of TaCOMT1A in flavonoid biosynthesis and drought resilience, highlighting its enzymatic activities in producing melatonin and sakuranetin. It also establishes the potential of melatonin and sakuranetin as eco-friendly agents to enhance wheat drought tolerance and productivity, paving the way for sustainable agricultural practices under water-limited conditions.