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Abstract
Bois noir is the most widespread phytoplasma grapevine disease in Europe. It is associated with ‘Candidatus Phytoplasma solani’, but molecular interactions between the causal pathogen and its host plant are not well understood. In this work, we combined the analysis of high-throughput RNA-Seq and sRNA-Seq data with interaction network analysis for finding new cross-talks among pathways involved in infection of grapevine cv. Zweigelt with ‘Ca. P. solani’ in early and late growing seasons. While the early growing season was very dynamic at the transcriptional level in asymptomatic grapevines, the regulation at the level of small RNAs was more pronounced later in the season when symptoms developed in infected grapevines. Most differentially expressed small RNAs were associated with biotic stress. Our study also exposes the less-studied role of hormones in disease development and shows that hormonal balance was already perturbed before symptoms development in infected grapevines. Analysis at the level of communities of genes and mRNA-microRNA interaction networks revealed several new genes (e.g., expansins and cryptdin) that have not been associated with phytoplasma pathogenicity previously. These novel actors may present a new reference framework for research and diagnostics of phytoplasma diseases of grapevine.
Highlights
Bois noir is the most widespread phytoplasma disease of grapevines (Vitis vinifera L.) in Europe and can lead regionally to losses of up to 50% [1]
The RNA-Seq analysis of samples from these grapevines revealed that there was not even a single differentially expressed gene defined between the recovered and uninfected grapevines (Table S1), which indicated that the recovery appeared to have occurred previously, in 2018 or 2019 [20]
Using a novel integrated analysis of transcriptomic data known as network enrichment methodology, which is based directly on RNA-Seq data [39], we explored the grouping of genes in communities that: (i) formed at the same times in the same groups of grapevines; and (ii) showed significant disintegration between the two growing seasons and between each group of grapevines (Figure 8, Table S6)
Summary
Bois noir is the most widespread phytoplasma disease of grapevines (Vitis vinifera L.) in Europe and can lead regionally to losses of up to 50% [1]. The interactions between grapevine and ‘Ca. P. solani’ have been extensively studied and are reviewed elsewhere [3]. As was proposed early in phytoplasma research, this accumulation is a consequence of the manipulation of the host metabolism by the phytoplasmas, which can turn infected plant tissues into a carbohydrate sink that provides phytoplasmas with hexoses [8,15,16]. Several studies have analyzed the expression of genes involved in carbohydrate metabolism and their enzyme products and sugar metabolites upon infection of grapevines with ‘Ca. P. solani’ [8,16,17,18,19,20]. Evidence points to important roles of the plant hormones in the signaling networks involved in grapevine responses to ‘Ca. P. solani’, the underlying molecular mechanisms of these interactions remain poorly understood [27]
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