Grapevine yellow mosaic is associated with stress-driven premature senescence and early photosynthetic decline

Yellow mosaic of grapevine (YM) manifests as an early yellowing of leaves and shoots at the beginning of the vegetation, often with a distinct mosaic pattern that typically fades as the season progresses. Although YM has long been associated with grapevine fanleaf virus (GFLV), the biological determinants of this phenotype remain unclear, and appear strongly modulated by cultivar and environmental conditions. To elucidate the molecular basis associated with this syndrome, high-throughput sequencing (HTS) of polyadenylated and small RNAs were conducted on YM–affected grapevine tissues, as well as on the green counterparts on the same plants, in June 2019. This was followed by a time-course sampling (May-September 2022) of the same plants or from plants of the same vineyards showing the comparable symptom, to validate the gene expression patterns.Virome characterization revealed a complex mixed infection in both yellow and green leaf tissues of the same individual plants, with multiple viral species identified across plants showing the same syndrome. Simultaneously, GFLV RT-qPCR quantification and the analysis of its molecular variants detected no significant differences in RNA titer or specific genetic variations between yellow and green leaf tissues, suggesting that GFLV RNA level alone is not the primary trigger for symptom expression.Transcriptomic profiling uncovered a metabolic reprogramming in yellow leaf tissues, characterized by strong downregulation of genes essential for photosynthesis and thylakoid structure, coupled with early induction of catabolic processes and stress-response pathways. These responses were mainly driven by protein kinases and activation of ABA synthesis and ethylene signalling. SmallRNA analysis further disclosed a coordinated shift in miRNA expression associated with stress adaptation. Transmission electron microscopy confirmed premature chloroplast dismantling in yellow tissues, including thylakoid disorganization and plastoglobule accumulation, hallmarks of leaf senescence.Overall, our findings reveal a finely tuned scenario in which YM phenotype does not primarily result from variations in viral load but rather may represent a host response to virus challenge(s) leading to premature senescence and an early functional collapse of the photosynthetic machinery.