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

Abstract

Wildfires are an increasingly urgent threat to viticulture, with smoke exposure leading to smoke taint, an off-flavor in wine characterized by undesirable "smoky" and "ashy" notes that can render grapes unmarketable and cause major economic losses. Smoke-derived volatile phenols (VPs) in grape berries, metabolized into stable, non-volatile glycoconjugates via glycosyltransferases (GTs), underlie smoke taint formation. Here, we present the dwarf grapevine cultivar Pixie as a model system for smoke taint research. We generated a haplotype-resolved, telomere-to-telomere diploid genome using HiFi long-read sequencing, along with an expression atlas spanning 30 replicated samples across various tissues and developmental stages. We also constructed a second telomere-to-telomere assembly for Pinot Noir to assess GT expression during berry ripening in the field. Controlled smoke-exposure experiments profiled GT expression and enabled transcriptome-wide analyses at multiple time points. We measured VPs in both smoke-exposed and control samples, revealing 12 GT1 genes significantly upregulated by smoke, named Vitis vinifera smoke-inducible UGTs (VviSIUGTs). Their expression peaked one day post-exposure and declined by day three, mirroring glycoside accumulation dynamics. Gene co-expression network analyses highlighted stress-responsive modules enriched in these VviSIUGTs, while transcription factor binding site analyses pinpointed stress-related regulatory elements in their promoters. Together, 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.

Keywords: Berry ripening; Pixie; genome assembly; grapevine; smoke taint; volatile phenol glycosylation; wild-fire smoke plant responses.