The Entry of Pollinating Fig Wasps Plays a Pivotal Role in the Developmental Phase and Metabolic Expression Changes in Ficus hookeriana Figs

The fig (the syconium of the Ficus tree) and its pollinating fig wasp represent exceptional examples for researching plant–insect interactions due to their remarkable specificity in species interaction and mutually beneficial symbiotic relationship. However, the mechanisms underlying the developmental process of monoecious figs in response to the entry of pollinating fig wasps (pollinators) and the metabolic changes occurring during this process remain elusive. Our study employed a combination of controlled experiments in the field and LC-MS methods to investigate the impact of pollinating fig wasp entry on the developmental phase of figs, as well as the metabolic alterations occurring during this process. A total of 381 metabolites and 155 differential metabolites were identified, with the predominant classes of metabolites being organic acids, lipids, and benzene aromatic compounds. The results suggest that in the absence of wasp entry, the receptive phase of fig would exhibit an extended duration. However, upon the entry of fig wasps, the receptive phase of figs would terminate within a span of 1 to 2 days, concomitant with substantial fluctuations in the composition and proportions of metabolites within the fig. Our research focuses on the analysis of linoleic acid metabolism, phenylpropanoid biosynthesis, and flavonoid biosynthesis pathways. Our findings suggest that the entry of wasps triggers alterations in the metabolic regulatory mechanisms of figs. Prior to wasp entry, metabolites primarily regulate fig growth and development. However, after wasp entry, metabolites predominantly govern lipid accumulation and the establishment of defense mechanisms, indicating a transition in fig development. This metabolic perspective explains why figs promptly enter an interflower phase that is not attractive to pollinating fig wasps after their entry, and how figs achieve reproductive balance through the regulation of different metabolic pathways. This study provides scientific evidence for elucidating the stability mechanism of the fig wasp mutualistic system.