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Background: Grapevine Trunk Diseases (GTD) threat worldwide wine and table grape production, mainly reducing grape yields and in advanced stages causing the death of diseased vines. A particular GTD of enormous concern in Argentinean vitiviniculture is the complex etiology disease locally known as "Hoja de malvón" (HDM). At least four different fungi are involved in the disease, which complicates the diagnostic and the design of strategies for vineyard management. Similar to Esca grape disease, factors that make this disease difficult to control are the presence of pathogens that not always correlates with disease symptoms or physiological changes in the host. Also the abiotic stress on grapevine seems to favors the disease process. Based on this background, it is essential to have molecular tools that allow for simultaneous explorations of the host immunity status and the microbiome composition. Results: A metatranscriptomic approach was followed and different strategies for microbiome characterization, throughmolecular marker reconstruction or unique kmer counts, were evaluated. Malbec microbiome was mainly represented for Dothideomycetes and Actinobacteria. Higher Basidiomycota/Ascomycota ratio was found in symptomatic (SYM) than in asymptomatic (ASYM) plants, with the Basidiomycota Arrambaria destruens found in higher levels in SYM plants. Besides, from mRNA-derived reads, the host functional status and main microbial functions based on gene expression were evaluated. Stress-tolerance mechanisms were activated on ASYM plants, being spermidine synthesis one of the most important, while from the microbiome side, prokaryotic tricarboxylic acid pathways were the primary differential function in SYM plants. Conclusions: This is a pioneering work for the characterization of multi-kingdom endophytic microbiome in woody tissues of grapevine cv. Malbec. Several microorganisms with negative interaction with GTD pathogens were identified and can be further explored as biological control agents for HDM disease. The integral analysis employed suggests that measuring Basidiomycota/Ascomycota ratio and spermidine-associated gene expression would help to monitor the sanitary status of grapevine and the propensity to develop HDM disease. This study provides a departure point for a better comprehension of HDM disease that can be used as a roadmap for further development of curative practices of GTD.