Arbuscular mycorrhizal fungi modify temporal virus accumulation and distribution in different grapevine tissues

Arbuscular mycorrhizal fungi (AMF) have been shown to improve plant host tolerance to biotic stresses. However, AMF-mediated protection against virus diseases have been highly variable and poorly investigated in perennial crops. In this study, we investigated the influence of AMF on virus concentration and distribution in grapevine coinfected with three common viruses, grapevine rupestris stem-pitting associated virus (GRSPaV), solely or in coinfection with grapevine leafroll-associated virus 3 (GLRaV-3) and grapevine Pinot Gris virus (GPGV). Two different types of AMF inocula were used: i) Rhizophagus irregularis (Ri) and ii) R. irregularis, Funneliformis mosseae and F. caledonium (Mix). Sampling for quantitative RT-PCR (RT-qPCR) was performed three times throughout one-year period in four distinct grapevine tissues for the assessment of GRSPaV concentration in AMF-inoculated grapevine. AMF influence on GRSPaV was the most significant in the first sampling, two months post inoculation, with virus accumulating predominantly in roots. Simultaneously, GRSPaV concentration in young grapevine leaves was low, possibly due to modified source-sink dynamics. Quantification of GLRaV-3 and GPGV was performed in coinfected grapevine in the third sampling. After a year, both viruses exhibit accumulation in the roots of mycorrhizal plants. However, GLRaV-3 displayed accentuated accumulation and GPGV decrease in foliage, indicating differential effect on the virus in coinfected grapevine. Regarding AMF symbiosis, generally Mix inoculum induced more pronounced virus concentration changes than Ri alone. In summary, this study shows differences in virus load of AMF-inoculated and AMF-free grapevine and adds nuance to the complex multitrophic interactions that are shaping grapevines health.