Integrated multi-omics reveals terpenoid-driven metabolic and transcriptional regulation underlying sweetpotato resistance to black spot disease

Sweetpotato black spot disease, caused by the fungus Ceratocystis fimbriata , is known to have a detrimental impact on both crop yield and postharvest quality. This research employed a combination of transcriptomic and metabolomic analyses to explore the mechanisms of disease resistance in the black spot-resistant cultivar SS23 and the susceptible cultivar GS08. SS23 exhibited milder symptoms with reduced lesion severity, while GS08 displayed significant root damage. The integrated multi-omics approach revealed that SS23 upregulated defense-related genes (e.g., peroxidase, chitinase) and underwent metabolic reprogramming, leading to the accumulation of resistance-associated metabolites such as leucine, proline, and sesquiterpenoids like plumericin. In contrast, GS08 exhibited transcriptional stagnation and suppressed amino acid metabolism. The comprehensive analysis highlighted the importance of terpenoid biosynthesis: SS23 orchestrated the activity of terpene synthases ( IbTPS ) and cytochrome P450s to enhance the production of antifungal metabolites, while GS08 predominantly upregulated genes in the mevalonate pathway ( IbHMGR ) without downstream specialization. Through volatile profiling, 13 novel terpenoids were identified in SS23 post-infection (including isoterpinolene), in comparison to six in GS08. Notably, the compounds specific to SS23 demonstrated robust antifungal properties. The tightly interconnected gene-metabolite networks in SS23 effectively contained the pathogen, whereas the metabolic dysregulation in GS08 strongly correlated with disease susceptibility. This study underscores the importance of terpenoid pathway manipulation in the development of black spot-resistant sweetpotato varieties, with the identified core genes serving as potential molecular markers for precision breeding strategies.