Biological and molecular interplay between two viruses and powdery and downy mildews in two grapevine cultivars

Abstract

Grapevine may be affected simultaneously by several pathogens whose complex interplay is largely unknown. We studied the effects of infection by two grapevine viruses on powdery mildew and downy mildew development and the molecular modifications induced in grapevines by their multiple interactions. Grapevine fanleaf virus (GFLV) and grapevine rupestris stem pitting-associated virus (GRSPaV) were transmitted by in vitro-grafting to Vitis vinifera cv Nebbiolo and Chardonnay virus-free plantlets regenerated by somatic embryogenesis. Grapevines were then artificially inoculated in the greenhouse with either Plasmopara viticola or Erysiphe necator spores. GFLV-infected plants showed a reduction in severity of the diseases caused by powdery and downy mildews in comparison to virus-free plants. GFLV induced the overexpression of stilbene synthase genes, pathogenesis-related proteins, and influenced the genes involved in carbohydrate metabolism in grapevine. These transcriptional changes suggest improved innate plant immunity, which makes the GFLV-infected grapevines less susceptible to other biotic attacks. This, however, cannot be extrapolated to GRSPaV as it was unable to promote protection against the fungal/oomycete pathogens. In these multiple interactions, the grapevine genotype seemed to have a crucial role: in ‘Nebbiolo’, the virus-induced molecular changes were different from those observed in ‘Chardonnay’, suggesting that different metabolic pathways may be involved in protection against fungal/oomycete pathogens. These results indicate that complex interactions do exist between grapevine and its different pathogens and represent the first study on a topic that still is largely unexplored.

Modifications of Grapevine Berry Composition Induced by Main Viral and Fungal Pathogens in a Climate Change Scenario

“…This highly interesting observation was somehow confirmed in a very elegant experiment, where authors transmitted GFLaV and grapevine rupestris stem pitting-associated virus (GRSPaV), by in vitro -grafting, to Nebbiolo and Chardonnay. Upon subsequent downy and powdery mildew infection, GFLV-infected plants showed a reduction in severity of the diseases caused by powdery and downy mildews in comparison to virus-free plants, which highlights a potential upregulation of plant innate immunity by GLRD infection ( Gilardi et al, 2020 ).…”

Secondary Metabolism and Defense Responses Are Differently Regulated in Two Grapevine Cultivars during Ripening

“…In our dataset, VvWRKY18 (VIT_04s0008g05760) was strongly expressed in ‘Nebbiolo’ at E-L31, and then its transcriptional rates decreased during ripening, while in ‘Barbera’, the expression levels of this gene were constant at all sampling times ( Figure 3 ). Interestingly, the constitutive high basal expression of VvWRKY18 in ‘Nebbiolo’ was also observed by analyzing the leaves of this cultivar in comparison to ‘Chardonnay’ [ 58 ].…”

“…In addition to specific transcription factors, sugars involved in the priming of plant defense responses can modulate defense-related genes [ 59 ]. For instance, the sugar transporter VvSTP13 (VIT_05s0020g03140), which is involved in intracellular glucose uptake, was associated with defense responses in particular rootstock–scion combinations [ 14 ] and in response to fungal infection [ 58 ]. We found that, independently of the year, VvSTP13 was overexpressed in ‘Nebbiolo’ berries at E-L31, while in ‘Barbera’, it was particularly induced at E-L38 ( Figure 3 ).…”

“…Therefore, during ripening, ‘Nebbiolo’ grapes showed a stronger constitutive expression of defense genes than ‘Barbera’, with the exception of the harvest stage, when other molecular regulatory signaling, mainly correlated with anthocyanin accumulation, probably occurred [ 13 ]. Notably, the high basal expression of stress-responsive genes in ‘Nebbiolo’ was also documented in leaves infected by powdery mildew and subjected to elicitor applications [ 16 ] as well as in leaves infected by viruses [ 58 ]. In addition, several cultivar-associated genes, specific of the ‘Nebbiolo’ genome and involved in response to pathogens, were previously identified [ 26 ].…”

“…In addition, several cultivar-associated genes, specific of the ‘Nebbiolo’ genome and involved in response to pathogens, were previously identified [ 26 ]. This genotype-specific regulation of defense responses may also constitute an important ecological advantage, as it may result in reduced accumulation of harmful viruses, such as grapevine fanleaf virus [ 58 ], as well as in low titers and mild symptoms of Flavescence dorée phytoplasma [ 60 , 61 ], thus making ‘Nebbiolo’ more resilient than other cultivars (e.g., ‘Barbera’) to environmental and biotic constraints.…”