Integrated metabolome and transcriptome analysis elucidates reproductive functional divergence and regulatory mechanisms underlying the distinct spatial distribution of female flowers in monoecious figs

Abstract

Ficus plants and their pollinating fig wasps have developed a highly specific mutualistic relationship. Figs rely exclusively on their specialized wasps for pollination, while the wasps can only complete their reproductive cycle within the figs. Nevertheless, both fig seed production and the pollinator's offspring development depend on the same pool of female flowers within monoecious fig, which results in competition for the allocation of reproductive resources. Currently, the internal regulatory mechanisms underlying the functional differentiation of female flowers remain poorly understood. To address this gap, our study integrates transcriptomic and metabolomic analyses of the monoecious fig species Ficus hookeriana to investigate molecular and metabolic variations in female flowers with distinct reproductive functions and spatial distributions across three developmental phases: pre-female, female, and inter-floral phases. Results indicate that during the pre-female phase, spatially distinct female flowers exhibit differences in nucleotide metabolism-related processes, suggesting an early divergence in molecular programs associated with reproductive functional differentiation. During the female phase, Pollinator entry is associated with spatial variation in flavonoid biosynthesis-related metabolites and gene expression patterns, which may account for inter-individual differences in defense-related chemical profiles among female flowers. During the inter-floral phase, differential accumulation of metabolites and changes in gene expression in the TCA cycle pathway suggest altered energy metabolism and carbon resource utilization, potentially contributing to the balance between seed development and wasp gall formation. This study systematically elucidates stage-specific metabolic and transcriptional variation associated with reproductive resource partitioning in monoecious figs, offering omics-based insights into the molecular basis underlying the functional differentiation of female flowers and advances our understanding of the metabolic processes associated with plant–insect mutualistic interactions.