Abstract
Phaeomoniella chlamydospora is a tracheomycotic fungus that colonizes the xylem of grapevines (Vitis vinifera L.), causing wood discoloration, brown wood streaking, gummosis, and wood necrosis, which negatively affect the overall health, productivity, and life span of vines. Current control strategies to prevent or cope with P. chlamydospora infections are frequently ineffective. Moreover, it is unclear how fungicides commonly applied in vineyards against downy and powdery mildew agents affect the wood mycobiome, including wood pathogens such as P. chlamydospora. In this study, we used next-generation sequencing to assess the effects of foliar spray of grapevines with inorganic (copper oxychloride and sulfur), synthetic (penconazole and fosetyl-aluminum), and natural (Blad) fungicides currently used against the downy and powdery mildews. The subjects of our investigation were (i) the resident wood mycobiome, (ii) the early colonization by a consortium of fungal wood endophytes (ACEA1), (iii) the wood colonization success of P. chlamydospora, and (iv) the in planta interaction between P. chlamydospora and ACEA1, under greenhouse conditions, in rooted grapevine cuttings of cv. Cabernet Sauvignon. The data obtained suggest that the resident mycobiome is affected by different fungicide treatments. In addition, the early colonization success of the endophytes composing ACEA1 varied in response to fungicides, with relative abundances of some taxa being overrepresented or underrepresented when compared with the control. The wood colonization by P. chlamydospora comported significant changes in the mycobiome composition, and in addition, it was greatly affected by the foliar spray with Blad, which decreased the relative abundance of this pathogen 12-fold (4.9%) when compared with the control (60.7%) and other treatments. The presence of the pathogen also decreased considerably when co-inoculated into the plant with ACEA1, reaching relative abundances between 13.9% and 2.0%, depending on the fungicide treatment applied. This study shows that fungicides sprayed to prevent infections of powdery and downy mildews have an effect on non-target fungi that colonize the endosphere of grapevines. We suggest two potential control strategies to fight P. chlamydospora, namely, the foliar spray with Blad and the use of ACEA1. Further studies to confirm these results are required.
Highlights
Protecting grapevines (Vitis vinifera L.) from fungal pests by means of fungicides dates back to the late 1800s, with the accidental discovery that a mixture of copper sulfate and lime, sprayed on vine leaves, was able to deter thieves from stealing grapes and able to prevent downy mildew infections (Morton and Staub, 2008)
Plants inoculated with P. chlamydospora presented extensive wood discoloration (Category 3; Figures 2C, D), under all spray treatments, while mild to absent symptoms, such as those shown in Figures 2A, B were recorded when P. chlamydospora was inoculated along with ACEA1
This study shows that some common fungicides that have been applied in viticulture for decades affect the resident mycobiome and/or the wood colonization success of some endophytes, while leaving nearly unaffected the wood pathogen P. chlamydospora
Summary
Protecting grapevines (Vitis vinifera L.) from fungal pests by means of fungicides dates back to the late 1800s, with the accidental discovery that a mixture of copper sulfate and lime, sprayed on vine leaves, was able to deter thieves from stealing grapes and able to prevent downy mildew infections (Morton and Staub, 2008). The development of pathogen resistance pushed the search of ever more effective chemicals capable of dealing with increasingly resilient species (Verweij et al, 2009). It was only in recent years, with the advent of molecular ecology and its tools, such as metagenomics and metabarcoding, that scientists have begun to understand how fungicides, along with herbicides and insecticides, impact the microbial ecology of environments with unpredictable medium- and long-term consequences (Komárek et al, 2010; Setati et al, 2012; Karlsson et al, 2014; Morrison-Whittle et al, 2017). The vineyard is an extremely diverse environment, characterized by complex interactions among plants, soil microbes, endophytes, and epiphytes, which are associated with grapevine health (Zarraonaindia and Gilbert, 2015; Jayawardena et al, 2018) and with the concept of terroir, as it is a source of yeasts and bacteria especially important in winemaking (Pretorius et al, 1999; Setati et al, 2012)
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