Grapevine trunk diseases (GTDs) are currently among the most important health challenges for viticulture in the world. Esca, Botryosphaeria dieback, and Eutypa dieback are the most current GTDs caused by fungi in mature vineyards. Their incidence has increased over the last two decades, mainly after the ban of sodium arsenate, carbendazim, and benomyl in the early 2000s. Since then, considerable efforts have been made to find alternative approaches to manage these diseases and limit their propagation. Biocontrol is a sustainable approach to fight against GTD-associated fungi and several microbiological control agents have been tested against at least one of the pathogens involved in these diseases. In this review, we provide an overview of the pathogens responsible, the various potential biocontrol microorganisms selected and used, and their origins, mechanisms of action, and efficiency in various experiments carried out in vitro, in greenhouses, and/or in vineyards. Lastly, we discuss the advantages and limitations of these approaches to protect grapevines against GTDs, as well as the future perspectives for their improvement.

Two major diseases that affect grapevine leaves and berries are controlled by the oomycete Pythium oligandrum. As the efficacy of biocontrol agents strongly depends on factors such as the trophic behaviors of pathogens and cultivar susceptibility, a two-disease approach was implemented to evaluate the activity of P. oligandrum against Botrytis cinerea (the necrotrophic fungus of gray mold) and Plasmopara viticola (the biotrophic oomycete of downy mildew) on two grapevine cultivars with different susceptibilities to these two pathogens. The results show that grapevine root inoculation with P. oligandrum significantly reduced P. viticola and B. cinerea infection on the leaves of the two cultivars, but with differences. This was observed when the relative expression of 10 genes was measured in response to each pathogen, and could be attributed to their lifestyles, i.e., biotrophic or necrotrophic, which are related to the activation of specific metabolic pathways of the plant. In response to P. viticola infection, genes from the jasmonate and ethylene pathways were mainly induced, whereas for B. cinerea, the genes induced were those of the ethylene–jasmonate pathway. The different levels of defense against B. cinerea and P. viticola could also explain the difference in cultivar susceptibility to these pathogens.

Ascomycetes, basidiomycetes and deuteromycetes can degrade wood, but less attention has been paid to basidiomycetes involved in Esca, a major Grapevine Trunk Disease. Using a wood sawdust microcosm system, we compared the wood degradation of three grapevine cultivars inoculated with Fomitiporia mediterranea M. Fisch, a basidiomycete responsible for white-rot development and involved in Esca disease. The grapevine cultivar Ugni blanc was more susceptible to wood degradation caused by F. mediterranea than the cultivars Cabernet Sauvignon and Merlot. Solid-state Nuclear Magnetic Resonance (NMR) spectroscopy showed that F. mediterranea preferentially degrades lignin and hemicellulose over cellulose (preferential, successive or sequential white-rot). In addition, co-inoculation of sawdust with two cellulolytic and xylanolytic bacterial strains of Paenibacillus (Nakamura) Ash (Paenibacillus sp. (S231-2) and P. amylolyticus (S293)), enhanced F. mediterranea ability to degrade Ugni blanc. The NMR data further showed that the increase in Ugni blanc sawdust degradation products was greater when bacteria and fungi were inoculated together. We also demonstrated that these two bacterial strains could degrade the wood components of Ugni blanc sawdust. Genome analysis of these bacterial strains revealed numerous genes predicted to be involved in cellulose, hemicellulose, and lignin degradation, as well as several other genes related to bacteria-fungi interactions and endophytism inside the plant. The occurrence of this type of bacteria-fungus interaction could explain, at least in part, why necrosis develops extensively in certain grapevine varieties such as Ugni blanc.

Grapevine trunk diseases (GTDs) are currently limiting grapevine productivity in many vineyards worldwide. As no chemical treatments are registered to control GTDs, biocontrol agents are being tested against these diseases. Esquive^® WP, based on the fungus Trichoderma atroviride I-1237 strain, is the first biocontrol product registered in France to control GTDs. In this study, we determine whether, following grapevine pruning wound treatments with Esquive^® WP, changes occurred or not in the indigenous microbial communities that are colonizing grapevine wood. Over a 6-year period, Esquive^® WP was applied annually to pruning wounds on three grapevine cultivars located in three different regions. Wood samples were collected at 2 and 10 months after the Esquive^® WP treatments. Based on MiSeq high-throughput sequencing analyses, the results showed that specific microbial communities were linked to each ‘region/cultivar’ pairing. In certain cases, a significant modification of alpha diversity indexes and the relative abundance of some microbial taxa were observed between treated and non-treated grapevines 2 months after Esquive^® WP treatment. However, these modifications disappeared over time, i.e., 10 months post-treatment. This result clearly showed that Esquive^® WP pruning wood treatment did not induce significant changes in the grapevine wood’s microbiome, even after 6 years of recurrent applications on the plants.

Bacteria naturally colonize grapevine wood, and some populations interact synergistically with fungal pathogens to promote wood degradation. In this study, we characterized a bacterial strain, designated S150 ^T , isolated from the wood of grapevine cultivar Sauvignon Blanc. The strain was previously known as promoting wood degradation caused by the causal agent of white-rot, Fomitiporia mediterranea . Phylogenetic analysis based on the full-length 16S rRNA gene sequence showed that the strain S150 ^T belonged to the genus Paenibacillus . Based on 16S rRNA gene sequences, S150 ^T shared low sequence similarity values (between 96.5 and 97.5%) with closed recognized members of the genus ( P. jilunlii Be17, P. tepidiphilus SYSU G01001, P. tengchongensis SYSU-G-01003, P. sonchi X19-5, P. helianthi P26E). The cell wall peptidoglycan of S150 contains meso-diaminopimelate. MK6 and MK7 are the two respiratory quinones. The main cellular fatty acids are iso-C _16:0 and anteiso-C _15:0 . The polar lipids are diphosphatidylglycerol, phosphatidylethanolamine, three amino phospholipids, two phospholipids and three polar lipids. The whole-genome is 7.45 Mb, with a G+C content of 52.54%. The average nucleotide identity (ANI) value between S150 ^T and the closely related Paenibacillus member ( P. sonchi X19-5) was 85.06%. Biochemical and physiological analyses revealed that strain S150 ^T has different characteristics from reference strains Paenibacillus spp.. Phenotypic, phylogenetic and chemotaxonomic analyses show strain S150 ^T is a novel species of the genus Paenibacillus , for which the name Paenibacillus xylinteritus is proposed.