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Plant-derived microRNAs as mediators of the acquisition of honeybee worker phenotype

A European honey bee (Apis mellifera) extracts nectar from an Aster flower using its proboscis. Tiny hairs covering the bee's body maintain a slight electrostatic charge, causing pollen from the flower's anthers to stick to the bee, allowing for pollination when the bee moves on to another flower. Credit:  Photo by John Severns.

Social insects, such as honeybees (Apis mellifera), provide fascinating examples of natural social structures. These insects have a well-defined caste system, whereby tasks are divided depending on the “social class”. Queen bees are characterized by their remarkable reproductive capacity, large body size, and a marked longevity. Given their reproductive capacity, the main role of the queen bees is to sustain the beehive colony. In contrast, worker bees, are mostly sterile and have short life spans. Their main role is to ensure a sustained food supply, act as nurse bees to the larvae produced by the queen bees, and to produce wax cells, which constitute the physical scaffold of the beehive. However, the factors determining differentiation into either queen or worker beers are not fully understood yet. At a molecular level, a protein called Target Of Rapamycin (TOR) plays a central role in stimulating queen-like phenotype in honey bees. Other factors, such as food type, are also necessary for determining the worker phenotype; for example, royal jelly (a glandular secretion produced by nurse bees) induces the development of queen bees, whereas “beebread”, a mixture of pollen and honey, stimulates the development of worker bees.

In a recent study published in PLoS Genetics, Kegan Zhu et al. demonstrated that plant-derived microRNAs are involved in the development of worker bees. The authors first demonstrated that beebread was particularly enriched in a total of 16 plant-derived microRNAs when compared to royal jelly, which was preferentially enriched in animal-derived microRNAs. microRNAs are short RNAs involved in suppressing gene expression, have a tremendous impact on many physiological features of plants and animals, including development. The authors then asked whether these 16 plant-derived microRNAs were involved in honey bee larvae development. They found that when honey bee larvae were fed with beebread enriched in a particular subset of plant-derived microRNAs, they displayed a significant impairment in growth, and emerged as adults with worker-like features, such as reduced weight, size, and decreased ovary size. Consistent with the hypothesis that plant microRNAs suppress the expression of honey bee messenger RNA (mRNA) targets, using a combination of computational and experimental approaches, the authors showed that a specific plant microRNA, miR-162a, can bind to the TOR mRNA, and suppress the expression of TOR protein, thereby favouring the acquisition of a worker-like phenotype.

Interestingly, the regulation of TOR protein expression mediated by plant microRNAs is not limited to social insects. The authors also provided evidence of a similar effect of plant miR-162a in reducing weight, length, and ovary and brood size in the non-social insect Drosophila. This provides strong evidence to support an evolutionarily conserved interaction between plants and insects potentially mediated by microRNAs. However, it is important to stress that plant microRNAs are not expected to be the sole factors mediating caste development in social insects, as other factors such as protein, sugars, p-coumaric acid and fatty acids, have all been also proposed to play a key role in this process. Nevertheless, taken together, this study uncovers a new layer of complexity in the development of a caste system in social insects, and provides strong evidence to support the hypothesis that proposes the existence of cross-kingdom social interactions and co-evolution partially mediated by microRNAs.

Reference: Zhu, K, et al. (2017). Plant microRNAs in larval food regulate honeybee caste development. PLoS Genetics, 13(8): e1006946.

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