Tomato yellow leaf curl Sardinia virus and its C4 protein prime tomato plants against drought stress and fungal infections

Plants can be subjected simultaneously to abiotic and biotic stresses, such as drought and viral infections. The possibility that viruses repay host plants for the damages caused by the infection, helping them to endure abiotic stresses has been described, underpinning the existence of common molecular networks that regulate the plant responses towards the stimuli provoked by biotic and abiotic stresses. Recently, begomoviruses causing the tomato yellow leaf curl disease in tomatoes were shown to increase heat and drought tolerance, possibly through the intervention of the viral C4 protein. Here, we elucidated how the begomovirus tomato yellow leaf curl Sardinia virus (TYLCSV) and its C4 protein overexpressed in transgenic tomato plants modulate physiological and molecular events in tomato plants. Combining morphometric and physiological parameters and hormone content with transcriptional analysis of genes involved in water-stress response and hormone metabolism, we assessed that TYLCSV infection and the overexpressed C4 protein delay the onset of stress-related features, improve the water use efficiency, and facilitate a rapid post-rehydration recovery of plants. Specific anatomical and hydraulic traits, rather than biochemical signals, support such increased drought stress resilience. Moreover, we observed that plants overexpressing C4 induced tolerance to Oidium neolycopersici, the agent of powdery mildew, not only counteracting symptoms, conidia adhesion and secondary hyphae elongation, but also changing the expression of the pathogenesis-related genes and phytohormone biosynthesis. Overall, the priming role exerted by TYLCSV and its C4 protein in the adaptation to abiotic and biotic stresses opens new perspectives in the management of the effects of climate change in horticultural crops.