Integrative genome and transcriptome analysis identifies smoke-responsive glycosyltransferases in grapevine berries

Wildfires pose a growing threat to viticulture, with smoke exposure causing smoke taint-off-flavors described as 'smoky' or 'ashy' that can make grape unmarketable. This taint results from smoke-derived volatile phenols (VPs) absorbed by grape berries and converted into stable glycoconjugates via glycosyltransferases (GTs). We present the dwarf grapevine cultivar Pixie as a model system for smoke taint research. Using HiFi long-read sequencing, we produced a haplotype-resolved, telomere-to-telomere (T2T) diploid genome and a tissue- and stage-resolved expression atlas across 30 replicated samples. We constructed a second T2T assembly for Pinot Noir to assess GT expression during berry ripening in the field. Controlled smoke exposure experiments, combined with transcriptomics and VP quantification, revealed 12 GT1 genes highly up-regulated by smoke. We designated these as Vitis vinifera smoke-inducible UGT (VviSIUGT) genes. Their expression peaked 1 d post-exposure and declined by day 3, mirroring glycoside accumulation dynamics. Gene co-expression network analyses highlighted stress-responsive modules enriched in these VviSIUGT genes, while transcription factor-binding site analyses pinpointed stress-related regulatory elements in their promoters. These findings uncover early transcriptional responses to smoke in grape berries and identify candidate genes that can serve as molecular markers or engineering targets for developing grapevine cultivars with reduced susceptibility to smoke taint.