RNA localization in the honeybee (Apis mellifera) oocyte reveals insights about the evolution of RNA localization mechanisms

Subcellular localization of RNAs is a critical biological process for generation of cellular asymmetries for many cell types and a critical step in axis determination during the early development of animals. We have identified transcripts localized to the anterior and posterior of honeybee oocyte using laser capture microscopy and microarray analysis. Analysis of orthologous transcripts in Drosophila indicates that many do not show a conserved pattern of localization. By microinjecting fluorescently labeled honeybee transcripts into Drosophila egg chambers we show that these RNAs become localized in a similar manner to their localization in honeybee oocytes, indicating conservation of the localization machinery. Thus while the mechanisms for localizing RNA are conserved, the complement of localized RNAs are not. We propose that this complement of localized RNAs may change relatively rapidly through the loss or evolution of signal sequences detected by the conserved localization machinery, and show this has occurred in one transcript that is localized in a novel way in the honeybee. Our proposal, that the acquisition of novel RNA localization is relatively easy to evolve, has implications for the evolution of symmetry breaking mechanisms that trigger axis formation and development in animal embryos.

► Discovery of novel maternally localized RNAs in the honeybee oocyte.
► Lack of conservation of RNA localization patterns between orthologous RNAs.
► Drosophila oocytes are able to recognize and localize Apis mRNA transcripts.
► The RNA cargo evolves more rapidly than the localization machinery.
► RNA localization evolution permits co-option of new factors into axis patterning.