GLRaV-3 infection induces a metabolic reconfiguration of sugar transport and secondary metabolism in Vitis vinifera cv. Malbec

Abstract

Grapevine leafroll-associated virus 3 (GLRaV-3) represents a significant threat to viticultural productivity. This study analyzed the impact of this pathogen on the expression of genes involved in hexose transport and flavonoid biosynthesis in leaves of Malbec, a cultivar of great enological importance. Research was conducted on a vineyard located at the Mendoza Agricultural Experiment Station of the National Institute of Agricultural Technology (INTA). Using RT-qPCR, we evaluated the expression of HT1 (active hexose transporter), F3H1 (flavanone 3-hydroxylase), FLS1 (flavonol synthase), and F3’H and F3’5’H (flavonoid 3′-hydroxylase and 3’5′-hydroxylase, responsible for the synthesis of di- and tri-hydroxylated anthocyanins, respectively). Evaluations were performed in leaf tissues of healthy and GLRaV-3-infected plants at four phenological stages: pea-size berry, veraison, 18° Brix, and 24° Brix.

Results revealed that at veraison, infected plants showed overexpression of HT1, F3H1, and FLS1, suggesting an early activation of hexose transport compensation and antioxidant defenses in response to viral-induced stress. As veraison marks the onset of active secondary metabolite transport from source to sink, this compensation is likely linked to sugar accumulation in leaves due to phloem transport defects. In later stages, lower expression of F3’5’H and F3’H indicated altered biosynthesis of di- and tri-hydroxylated anthocyanins. Tri-hydroxylated synthesis was the first to be affected at 18° Brix, coinciding with visual leafroll symptoms.

These expression changes may be related to a redirection of carbon fluxes toward other metabolic pathways or to the inhibition of key enzymes in the flavonoid pathway. These metabolites are energetically expensive for the plant. When combined with accumulated oxidative damage in the photosynthetic apparatus, normal leaf function is impaired, affecting berry phenolic accumulation. These findings suggest that GLRaV-3 infection induces a complex metabolic reconfiguration in Malbec grapevines. Understanding the molecular mechanisms underlying these plant-pathogen interactions is crucial for developing sustainable management strategies and elucidating how the virus disrupts source-to-sink metabolite transport.