Impacts of Sodium Arsenite on Wood Microbiota of Esca-Diseased Grapevines

Abstract

Although sodium arsenite was widely used in Europe until its ban in 2003, its effects on microorganisms is not clearly understood. To improve our understanding of sodium arsenite curative effect on GTDs, grapevines displaying esca-foliar symptoms from different French regions (Alsace, Champagne, Languedoc) were treated or not with sodium arsenite, and analyzed for their wood microbiota. Using metabarcoding, we identified the fungal and bacterial taxa composition of microbiota colonizing woody trunk tissues. Large differences in fungal microbiota composition between treated and untreated grapevines were observed while no major impacts were observed on bacteria microbiota. The main fungal species detected in untreated necrotic woody tissues was Fomitiporia mediterranea (63–94%), a fungal pathogen associated with esca. The relative abundance of this fungal species significantly decreased after sodium arsenite treatment in the three vineyards, in particular in white-rot necrotic tissues and their borders (−90%). F. mediterranea was the most sensitive to sodium arsenite among fungi from grapevine woody tissues. These results strongly suggest that the effect of sodium arsenite on GTDs is due to its ability to efficiently and almost specifically eliminate F. mediterranea from white-rot necrotic tissues, allowing saprobic fungi to colonize the tissues previously occupied by this pathogenic fungus.

White Rot Fungi (Hymenochaetales) and Esca of Grapevine: Insights from Recent Microbiome Studies

“…As suggested by Bruez et al [ 78 ], competition-induced metabolites may be good candidates for explaining leaf symptoms. Hypothetically, environmental perturbations in the plant-fungi interaction dynamics (with a possible involvement of bacteria [ 77 , 79 , 82 ]) may trigger the release of such chemicals that reach the canopy and lead to tiger stripes.…”

“…In a second study, Bruez et al [ 78 ] examined the effect of sodium arsenite on the endophytic mycobiome of leaf-symptomatic vines. Upon inspection, white rot was present in the stem of 60 to 100% of leaf-symptomatic plants, in three different vineyards.…”

“…In fact, field evaluations and, to a lesser extent, pathogenicity tests suggest that both the presence of white rot fungi and tracheomycotic Ascomycetes is necessary to trigger the expression of leaf symptoms. Besides, Pch does not seem to be significantly affected by sodium arsenite [ 78 ], and if this fungus alone was responsible for tiger stripes in leaves, it is hard to motivate how this treatment (or trunk surgery) effectively prevented symptom manifestation. The next question that naturally arises is: Can we control tiger stripes’ manifestation exclusively by targeting Fmed (or other white rot fungi)?…”

“…Among the numerous points in favor of culture-independent methods, NGS studies allow insights over unculturable and rare taxa, largely overcoming the cultural methods bias, and provide reasonable estimates for microorganisms' relative abundances [75]. Over the last three years, four NGS-based studies investigated the microbial ecology of esca proper-affected plants [76][77][78][79]. We hereby report some of the main findings and later discuss how they improve the state-of-the-art, over the involvement of white rot fungi in esca symptoms in leaves.…”

“…Treating vines with sodium arsenite successfully controlled esca for decades and, up until recently, its mode-of-action was unknown. Today, we know that this chemical affects the plants physiology and microbial ecology, successfully preventing leaf symptoms' manifestation [15,78]. Similarly, trunk surgery, an ancient practice recently rediscovered, is capable of strongly reducing the expression of leaf symptoms for several years after treatment [18,79].…”