A multi-omics comparative analysis reveals differential responses of epiphytic and terrestrial orchids in Cymbidium to waterlogging

Waterlogging stress is a major abiotic constraint that impedes plant growth and development by inducing root hypoxia, metabolic imbalances, and oxidative damage. Orchids, valued as important ornamental and medicinal plants, are highly susceptible to waterlogging, which frequently leads to severe root rot, as observed in field investigations and cultivation practices. Orchids include both epiphytic and terrestrial species that occupy habitats with pronounced differences in water availability. While the drought adaptation mechanisms of these two orchid life-forms have been extensively studied, the strategies underlying their adaptation to waterlogging remain poorly understood. Here, we investigated the responses of terrestrial Cymbidium sinense and epiphytic C. tracyanum to waterlogging stress using integrated physiological, metabolomic, and transcriptomic analyses. Under waterlogging stress, C. tracyanum suffered more severe morphological and ultrastructural damage compared to C. sinense, as well as greater rhizosphere hypoxia, reduced root activity, depletion of soluble sugars, and higher oxidative stress. Metabolomic and transcriptomic analyses revealed fundamentally divergent strategies between the species. C. sinense preferentially accumulated primary metabolites, particularly lipids, and specifically up-regulated genes related to triacylglycerol biosynthesis and UDP-glycosyltransferases. Integrated multi-omics analysis confirmed its reliance on enhanced primary metabolic pathways, such as alanine, aspartate, and glutamate metabolism, as well as linoleic acid metabolism, supporting waterlogging resilience. In contrast, C. tracyanum accumulated a diverse array of secondary metabolites and relied extensively on pathways such as phenylpropanoid and tyrosine metabolism. This high-investment strategy may have underlain its heightened sensitivity to waterlogging stress. Collectively, our findings provide mechanistic insights into the differential waterlogging responses between terrestrial and epiphytic Cymbidium species, thus offering perspectives on their adaptation and evolution while informing improved cultivation strategies.