Leveraging transcriptional, genomic, and epigenetic regulatory layers to enhance abiotic stress resilience in grapevine

Abstract

Grapevine (Vitis vinifera), an industry valued at approximately 108.61 billion US dollars globally, faces escalating threats from abiotic stresses that intensify under climate change and increasingly compromise berry quality, phenology, and yield. Despite decades of molecular characterization, translating stress biology knowledge into climate-resilient cultivars remains limited. We argue this gap reflects not a lack of knowledge within individual biological layers, but a fundamental failure to integrate across them. Grapevine stress tolerance operates through three interconnected regulatory layers. Transcription factor networks, WRKY, NAC, MYB, DREB, and bZIP families, constitute the most rapid layer, converging on shared ABA-mediated signaling hubs despite apparent stress-type specificity. Quantitative trait loci and genome-wide association studies capture the genomic architecture underlying these responses, yet remain critically under characterized for drought, salinity, and heavy metal tolerance. Epigenetic regulation through DNA methylation, histone modifications, and stress memory mechanisms constitutes a temporally durable third layer, uniquely important for perennial crops where adaptive chromatin states persist across growing seasons. Critically, these layers are not independent: transcription factor activity shapes the chromatin landscape, epigenetic marks modulate QTL expression, and genomic loci encode the regulatory machinery executing stress responses. Current breeding tools, marker-assisted selection, CRISPR/Cas9, and epigenomic selection, map onto these three layers but are overwhelmingly applied in isolation, limiting their collective impact. This review synthesizes knowledge gaps across all three layers within a unified hierarchical framework, arguing that deliberate cross-layer integration through multi-omics and precision breeding could enable cultivars capable of sustaining productivity under a rapidly changing climate.