Transcriptomic analysis of three fig (Ficus carica L.) genotypes reveals metabolic reprogramming during seasonal...

Seasonal development in perennial fruit species involves extensive metabolic modifications that support growth and environmental adaptation, but the molecular basis of coordination between primary and secondary metabolism in fig (Ficus carica L.) remains poorly characterized. To elucidate the seasonal regulation of metabolic pathways during syconium development, transcriptomic analyses were conducted on three fig genotypes (a caprifig, and two cultivars Dottato, and Petrelli) representing distinct reproductive types, sampled at two critical phenological stages (April and July) corresponding to breba growth and main crop development, respectively. Stringent pathway analysis of previously generated RNA-seq datasets highlighted a consistent metabolic reprogramming associated with both phenological stage and genotype differences, with pronounced modulation of biochemical pathways. Pathway filtering identified 15 pathways (45 unique genes) mainly associated with secondary metabolism and biosynthetic processes that showed higher expression in April (considered as up-regulated genes), and 23 pathways (79 unique genes) principally related to primary metabolism including photosynthesis and respiration that showed higher expression in July (considered as down-regulated genes). Among the pathways showing higher expression in July, photosynthesis-antenna proteins (map00196) and the tricarboxylic acid (TCA) cycle (map00020) exhibited the most consistent seasonal changes, with gene-level expression increasing 1.5- to 2.9-fold from April to July. A strong positive correlation (r = 0.77) between these pathways revealed tight coordination between light-harvesting capacity and central respiratory metabolism. Among the pathways showing higher expression in April, glucosinolate-, brassinosteroid-, and nucleotide-sugar-related processes were more highly expressed in April, while riboflavin metabolism increased in July, reflecting a shift from defense and growth functions in spring to energy-intensive metabolism during summer syconium development. Seasonal signals applied stronger and more uniform regulatory effects than genotypic or sex-related differences, though cultivar-specific metabolic characteristics were observed. Dottato exhibited the highest photosynthetic and respiratory gene expression in July, consistent with its robust parthenocarpic syconium development and ripening, while Caprifig displayed elevated TCA cycle activity potentially supporting specialized pollen production. These results revealed a fundamental metabolic architecture coordinating energy acquisition, respiratory activity, and biosynthetic processes during seasonal syconium development. The identified transcriptional networks provide molecular targets for breeding programs aimed at improving fig cultivation under changing environmental conditions.