Microbial succession from nursery to vineyard highlights the role of beneficial and pathogenic microbes in young vineyard yield

Abstract Background The grapevine microbiome plays a central role in shaping vineyard performance, yet the influence of nursery inherited microbes on vineyard establishment and early productivity remains poorly understood. Our goals were to study the endosphere and rhizosphere microbiome succession as grapevine transition from nursery to vineyard and determine in what capacity the endogenous microbiome from the nursery shapes vineyard outcomes. Results We profiled, using amplicon-based sequencing, the fungal and bacterial communities across five bio-compartments (scion graft union, rootstock graft union, crown, roots, and rhizosphere) from two sets of grafted vines (Cabernet Sauvignon and Chardonnay grafted on 1103P rootstock) originating from two nurseries and followed their succession over three years after planting in a commercial vineyard. Nurseries produced vines with distinct endospheric microbiomes that converged overtime but that remained significantly different after three years. Microbial turnover occurred at a much faster pace in belowground (root and rhizosphere) compared to trunk compartments post-planting, with 15% of the initial microbes persisting in three-year-old vineyard. The fungal pathobiome partially inherited from nurseries and associated with vascular diseases of the trunk and root was also clearly distinct after three years. Yet, we did not observe typical disease symptoms development or vine death as we would expect, likely because vines were not under stress during the experimental timeframe. Vineyard yield was highly variable among clonal vines, and statistical modeling revealed that a narrow subset of amplicon sequence variants (ASVs) explained a large portion of this variance. Regression models using the top ten high-impact ASVs accounted for 51% and 60% of yield variation in trunk and belowground compartments, respectively. Notably, 16 of the 19 yield-associated ASVs originated from nurseries, underscoring the long-term influence of nursery-derived microbes on vineyard success. Conclusion These findings highlight the dual role of beneficial and pathogenic nursery microbiota in shaping grapevine performance. It also suggests that the nursery life stage could be leveraged to engineer the grapevine microbiome and improve vineyard resilience.