Multi-omics profiling of high-carotenoid hybrid potato lines reveals coordinated metabolic reprogramming and associates with distinct tuber microbiota

Potato is a critical staple crop, and enhancing its carotenoid content is a promising strategy to improve its nutritional value. However, the synergistic mechanisms underlying carotenoid accumulation, superior nutritional traits, and the role of the endophytic microbiome remain unclear. Using an integrated multi-omics strategy, we systematically analyzed two high-zeaxanthin/lutein hybrids and four commercial cultivars. The hybrids accumulated significantly higher levels of zeaxanthin, lutein, and minerals, while exhibiting superior processing traits (e.g., higher dry matter/starch, lower reducing sugars). Integrated metabolomic and transcriptomic profiling revealed a coordinated upregulation of carotenoid and phenylpropanoid biosynthesis, alongside enrichment of stress-responsive phenolic acids. Notably, the endophytic microbiome in high-carotenoid tubers was distinct, dominated by Firmicutes and Proteobacteria, with genera like Bacillus and Latilactobacillus positively correlating with carotenoid content. Weighted gene co-expression network analysis identified a core regulatory module containing key genes (e.g., CCD4, BCH2) and novel transcription factors. Our findings elucidate a synergistic network linking metabolism, gene regulation, and the endophytic microbiome that collectively is associated with carotenoid accumulation and tuber quality. This provides critical targets for breeding nutritionally enhanced potatoes with desirable agronomic performance, supporting nutritional security and sustainable agriculture.