Giuseppe Ardagna, Sofia Gambini, Alessandra Bulgarini, Stefano Negri, Martino Bianconi, Flavia Di Carlo, Stefania Ceoldo, Flavia Guzzo, Mauro Commisso
Phenylpropanoids are specialized metabolites involved in multiple aspects of plant physiology and contribute to fruit quality and human health benefits. In sweet cherry (Prunus avium L.), metabolomic studies have largely focused on fruits, showing that cultivar identity contributes to phenylpropanoid pathway specialization. However, the contribution of genotype to phenylpropanoid organization in other organs, particularly leaves, remains poorly understood. Here, we applied an untargeted metabolomics approach to investigate genotype-associated phenylpropanoid pathway specialization in sweet cherry leaves, using fruits as a reference organ. Leaves and fruits from seven sweet cherry cultivars ("Early Bigi", "Burlat", "Sandra", "Grace Star", "Romana", "Durone Rosso", and "Ferrovia"), representing early-, mid- and late-ripening genotypes, were sampled at full fruit maturity across multiple orchards and over two consecutive growing seasons. Distinct organ-specific phenylpropanoid profiles were observed, with fruits characterized by the accumulation of anthocyanins, flavan-3-ols, and simple hydroxycinnamic acids, and leaves enriched in flavonols, hydroxycinnamic acids, and structurally diverse phenylpropanoid derivatives. Multivariate and univariate analyses identified cultivar identity as a major component of phenylpropanoid pathway specialization within each organ. Genotype-associated differences involved multiple phenylpropanoid subclasses and remained detectable across growing seasons and orchard locations. Overall, these findings indicate differential channeling of the phenylpropanoid pathway between fruits and leaves and show that, within the range of environmental conditions covered by the present experimental design, genotype-associated variation contributes to shaping phenylpropanoid composition in sweet cherry leaves, revealing a level of organization that had not been previously established in this organ.