VqBGH52 enhances the accumulation of trans-resveratrol through hydrolysis of trans-piceid and resistance to powdery mildew in Chinese wild grapevine

Abstract

Powdery mildew poses a significant threat to grapevine cultivation worldwide, resulting in increased production costs. Vitis quinquangularis accession ‘Danfeng-2’ accumulates high concentrations of stilbenes and exhibits resistance to powdery mildew. This study investigates the regulatory mechanisms of stilbene accumulation and disease-resistance in ‘Danfeng-2’ and V. vinifera cultivar ‘Cabernet Sauvignon’ grapevine following inoculation with Erysiphe necator. ‘Danfeng-2’ accumulates high levels of stilbenes at 3 days post-inoculation (dpi), whereas ‘Cabernet Sauvignon’ reaches peak accumulation by 5 dpi. Transcriptomic analysis revealed the upregulation of the gene VqBGH52 in ‘Danfeng-2’ specifically at 3 dpi, suggesting its role in disease resistance. The prokaryotically expressed VqBGH52 and VvBGH52 proteins efficiently hydrolyze trans-piceid into trans-resveratrol. These results are consistent with findings that genetically transformed lines overexpressing VqBGH52 exhibit enhanced resistance to E. necator, along with increased levels of trans-resveratrol, ε-viniferin, and pterostilbene, and reduced levels of trans-piceid. To uncover the mechanisms of the distinct expression of VqBGH52, we characterized its promoter and found that it contains an additional 1492-bp fragment compared to the VvBGH52 promoter. This fragment is associated with the rapid response of VqBGH52 upon E. necator inoculation in ‘Danfeng-2’, as well as the induction of disease resistance genes and those responding to SA, flg22, and chitin treatments. In conclusion, VqBGH52 hydrolyzes trans-piceid to generate trans-resveratrol, which subsequently serves as a substrate for producing toxic stilbenes such as ε-viniferin and pterostilbene. These findings elucidate the metabolic mechanisms through which VqBGH52 contributes to powdery mildew resistance by converting trans-piceid into toxic stilbenes.