Summary: Esca, a major grapevine trunk disease in old grapevines, is associated with the colonization of woody tissues by a broad range of plant pathogenic fungi. To identify which fungal and bacterial species are involved in the onset of this disease, we analysed the microbiota from woody tissues of young (10‐year‐old) grapevines at an early stage of esca. Using meta‐barcoding, 515 fungal and 403 bacterial operational taxonomic units (OTUs) were identified in woody tissues. In situ hybridization showed that these fungi and bacteria co‐inhabited in grapevine woody tissues. In non‐necrotic woody tissues, fungal and bacterial microbiota varied according to organs and seasons but not diseased plant status. Phaeomoniella chlamydospora , involved in the Grapevine trunk disease, was the most abundant species in non‐necrotic tissues from healthy plants, suggesting a possible non‐pathogenic endophytic behaviour. Most diseased plants (70%) displayed cordons, with their central white‐rot necrosis colonized essentially by two plant pathogenic fungi ( Fomitiporia mediterranea : 60%–90% and P. chlamydospora : 5%–15%) and by a few bacterial taxa ( Sphingomonas spp. and Mycobacterium spp.). The occurrence of a specific association of fungal and bacterial species in cordons from young grapevines expressing esca‐foliar symptoms strongly suggests that that microbiota is involved in the onset of this complex disease.

The worldwide increase in grapevine trunk diseases, mainly esca, represents a major threat for vineyard sustainability. Biocontrol of a pioneer fungus of esca, Phaeomoniella chlamydospora, was investigated here by deciphering the tripartite interaction between this trunk-esca pathogen, grapevine and the biocontrol-oomycete, Pythium oligandrum. When P. oligandrum colonizes grapevine roots, it was observed that the wood necroses caused by P. chlamydospora were significantly reduced. Transcriptomic analyses of plant and fungus responses were performed to determine the molecular events occurring, with the aim to relate P.chlamydospora degradation of wood to gene expression modulation. Following P. oligandrum-root colonization, major transcriptomic changes occurred both, in the grapevine-defense system and in the P. chlamydospore-virulence factors. Grapevine-defense was enhanced in response to P. chlamydospora attacks, with P. oligandrum acting as a plant-systemic resistance inducer, promoting jasmonic/ethylene signaling pathways and grapevine priming. P. chlamydospora pathogenicity genes, such as those related to secondary metabolite biosynthesis, carbohydrate-active enzymes and transcription regulators, were also affected in their expression. Shifts in grapevine responses and key-fungal functions were associated with the reduction of P. chlamydospora wood necroses. This study provides evidence of wood fungal pathogen transcriptional changes induced by a root biocontrol agent, P. oligandrum, in which there is no contact between the two microorganisms.

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.

Pruning experimental studies have been performed in different vineyards, in France, USA and Australia. This article investigates and models the effects of pruning quality on the installation of desiccation cones and wood necrotization. Two different modalities of pruning, short and high pruning, were performed at the same period each year on three cultivars in Bordeaux (Cabernet Sauvignon and Sauvignon Blanc) and Charente (Ugni Blanc) wine regions. In the short typ of pruning, the diaphragm was damaged but, in the high one, a 2–3 cm woody length was left immediately above the diaphragm. None of the three cultivars showed any correlation between necrosis length and spur diameter (R² < 0.1925). Analysis of the Ugni Blanc, 8 months after pruning, showed significantly more necrosis length (>60%) than either Cabernet Sauvignon (31–41%) or Sauvignon Blanc (25–55%). Desiccation cone necrotization rates also varied with the vintage, particularly for Ugni Blanc. 4 or 8 months after pruning, the newly-installed desiccation cones could then be analysed. High pruning stopped the desiccation cones at the diaphragm, which ensured that the sap flow path remained unaffected.

Grapevine curettage was re-introduced in France in the early 2000s, and is important for facilitating recovery of plants from esca disease. This surgical practice involves removal of deadwood of vines with leaf symptoms, focusing on white rot generally observed at the centres of grapevine trunks. Assessment of the efficacy of this practice was initiated in the Bordeaux region in 2014. One ‘Sauvignon Blanc’ vineyard severely affected by esca was initially surveyed in the summer of 2014, to identify and treat vines with esca foliar symptoms. Annually thereafter, from 2014 to 2018, selected vine stocks were curetted. Two other ‘Sauvignon Blanc’ vineyards also displaying high levels of esca damage were added to the study in 2015 and 2016. Curettage treatments ceased in 2018, resulting in 11 trials (vineyard × year combinations). In total, 856 vines (422 curetted and 434 control vines) were then surveyed annually up to 2021, for assessments and comparisons of esca development. At each site, plants with esca symptoms recovered well after curettage: on average 85% of all curetted vines became asymptomatic the year immediately after the treatment. Six years after treatment, for curettage campaigns carried out in 2014 and 2015, more than half of the curetted vines were symptom-free, whereas <12% of the control vines were asymptomatic, and gradual loss of efficacy was observed at each site. The mean annual proportion of efficacy erosion was approx. 8% per year. This study highlights the possible short- and mid-term benefits of trunk surgery to enable recovery of esca-affected vines, and for them to recover and remain leaf-asymptomatic for several years.