Honeybee larvae develop into workers but not queens, in part, because their diet of beebread/pollen is enriched in plant miRNAs. While miRNAs are generally negative regulators of gene expression in eukaryotes, they also negatively regulate larval development when honeybee larvae consume beebread/pollen and take up plant miRNAs. Xi Chen and Chen-Yu Zhang’s group in Nanjing University, report this finding on August 31, 2017 in PLOS Genetics.
How caste has formed in honeybees is an enduring puzzle. Although queens and workers are genetically identical, queens are reproductive and have a larger body size, develop faster and live longer than workers. Prevailing view is that differential larval feeding determines caste differentiation: royal jelly stimulates the differentiation of larvae into queen, whereas beebread and pollen consumed by the rest of the larvae lead to the worker bee fate. However, it is still not fully understood how alterations in diet modify so thoroughly the developmental trajectory of honeybees.
In previous studies, Chen-Yu Zhang’s group has reported a striking finding that plant miRNAs are ingested from plant diets and pass through the gastrointestinal tract, enter into the blood, accumulate in tissues and regulate endogenous gene expression in animals. Their findings suggest that ingested exogenous miRNAs can regulate endogenous gene expression and reshape animal phenotypes. Interestingly, since the components of beebread/pollen are mainly plant materials and royal jelly is a glandular secretion of nurse bees, the diets for worker- and queen-destined larvae are differentially derived from plant- and animal-sources. Therefore, Xi Chen, Chen-Yu Zhang and colleagues decide to investigate if miRNAs from different larval diets may have distinct impacts on honeybee development.
Here, they report that plant miRNAs are more enriched in beebread/pollen than in royal jelly. While plant miRNAs of beebread/pollen are fed to larvae, they cause developmental delay and reductions in body and ovary size in honeybees; in contrast, miRNAs in the royal jelly are not sufficient to reach a functional level, therefore queen-destined larvae evade this regulation. Mechanistic studies reveal that amTOR, a stimulatory gene in caste differentiation, is the direct target of miR162a. Interestingly, ingested plant miRNAs have a similar inhibitory effect on fruit fly development, even though fruit fly is not a social insect. In summary, this study uncovers a new mechanism that plant miRNAs in larval diet of worker bees delay caste differentiation and keep ovaries inactive, thereby inducing sterile worker bees.
The findings of this study are important for the following reasons: