Common mycorrhizal network transfers virus infection signals between neighboring grapevines

Abstract

Arbuscular common mycorrhizal networks (CMNs) allow plants to exchange signals, enabling responses to biotic and abiotic stresses in neighboring individuals. However, no studies documenting the transmission of signals from virus-infected plants through CMNs have been published so far. The aim of this study was to investigate whether virus-free grapevine plants, connected via CMNs to grapevines infected with grapevine leafroll-associated virus 3 (GLRaV-3), exhibit physiological or molecular responses to the neighboring virus infection. A three-year greenhouse experiment was conducted, in which virus-free and virus-infected grapevines were either connected or not via CMN. Five and fifteen months after AMF inoculation, we assessed oxidative stress markers, antioxidative enzyme activities, hormonal profiles, photosynthetic performance, pigment concentrations, growth parameters, and leaf nutrient content. In addition, expression levels of nine selected genes were measured at the second sampling. The virus-free receiver plants showed elevated levels of abscisic acid (ABA) and its derivate, phaseic acid (PA), as well as increased leaf magnesium concentrations, indicating a physiological response to the neighboring infection. The presence of CMN also influenced physiological traits in donor plants, particularly in ABA metabolism, antioxidant activity of ascorbate peroxidase, and leaf magnesium content, depending on their virus infection status. These findings provide novel evidence that grapevine plants can perceive viral stress in neighbouring plants through CMN connections, and highlight the important role of ABA signalling in these interactions. This research contributes to a deeper understanding of plant communication and stress perception, with potential implications for managing viral diseases in perennial crops.

Keywords: Abscisic acid; Grapevine leafroll-associated virus 3; Magnesium; Plant–microbes interaction; Rhizophagus irregularis; Virus-induced stress signalling; Vitis vinifera L..