Conditional mutualism between Grapevine rupestris stem pitting-associated virus and Vitis vinifera triggers drought tolerance.

Grapevine rupestris stem pitting-associated virus (GRSPaV) is a widely spread virus affecting Vitis spp. Although it establishes a compatible viral interaction in V. vinifera without the development of phenotypic alterations, it can occur as distinct variants that showed different symptoms on diverse Vitis species. In the present work, we analyzed the changes induced by GRSPaV in Vitis vinifera cv 'Bosco', an Italian white-grape variety, by combining agronomic, physiological and molecular approaches, in order to provide global information about the effects of GRSPaV. This virus induces a moderate decrease in physiological efficiency, yield performance and berry sugar content, associated to several transcriptomic alterations. Transcript changes were assessed by microarray analysis in petiole, leaf and berry samples collected at véraison, and by quantitative real-time RT-PCR. Global gene expression analyses showed some unexpected responses in grapevine never reported before for other plant-virus interactions, such as the increase in transcription of genes involved in photosynthesis and CO2 fixation associated to a moderate decrease in photosynthesis rate, the decrease of some defence mechanisms and overlapping responses to drought and salinity stresses. Basing on these last considerations, we hypothesized an interaction between GRSPaV-grapevine-drought and we subjected GRSPaV-free and infected plants to a drought treatment under controlled conditions. The virus changes grapevine responses to drought: GRSPaV-infected plants show higher stomatal opening, grow more than GRSPaV-free plants under water stress condition, and are able to extract more water from the soil. Furthermore, we prepared 4 libraries of small RNAs (GRSPaV-free and infected plants upon well watered and stress conditions), which were sequenced by Illumina technology. We observed a surprising profile of miRNAs associated with the presence of GRSPaV in plants upon water stress treatment. Viruses are obliged infectious entities and several studies have already showed that they may provide beneficial effects to the host in particular environmental conditions. We hypothesized that the long co-existence between grapevine and GRSPaV resulted in the evolution of a form of mutual adaptation between the virus and its host.