Metabolome–transcriptome integration reveals waterlogging tolerance pathways in Chrysanthemum morifolium

Waterlogging is one of the most detrimental abiotic stressors affecting the growth and development of Chrysanthemum morifolium. However, the vital metabolites and metabolic pathways that contribute to waterlogging tolerance in chrysanthemum remain to be investigated. In this study, we conducted a multiomics investigation of the metabolome and transcriptome of chrysanthemum after waterlogging treatment with the aim of exploring vital metabolites and their pathways related to waterlogging tolerance in chrysanthemum. Exposure to waterlogging stress for six days resulted in increased activities of key antioxidant enzymes and significant accumulation of both proline and malondialdehyde (MDA) in chrysanthemum. Twelve hours of waterlogging stress treatment resulted in rapid metabolome and transcriptome remodeling in chrysanthemum. A comparison of the control (CK-1 to CK-3) and waterlogging (W-1 to W-3) groups revealed a total of 86 differentially abundant metabolites (DMs), 28,010 differentially expressed genes (DEGs) and 122,961 lncRNAs (DELs). A total of 1115 differentially expressed transcription factors (DETFs) under waterlogging stress were distributed mainly in the ERF, bHLH, MYB and NAC families. Integrative transcriptomic and metabolomic analyses revealed that waterlogging stress substantially reprogrammed key metabolic pathways in chrysanthemum, with DEGs and DMs significantly enriched in starch and sucrose metabolism, the TCA cycle, cysteine and methionine metabolism, arginine and proline metabolism, linoleic acid metabolism and phenylpropanoid biosynthesis, suggesting that these pathways may be pivotal for the response of chrysanthemum to waterlogging stress. On the basis of these results, we constructed a putative DEL/DETF–DEG–DM regulatory network model, comprehensively revealing novel relationships governing transcriptional and metabolic regulation under waterlogging stress in chrysanthemum. This research provides significant insights into crucial metabolic pathways that regulate the waterlogging tolerance of chrysanthemum under waterlogging stress and presents effective guidance for the breeding of waterlogging-tolerant germplasms in chrysanthemum.