Synchronized Expression of Retinoid X Receptor mRNA with Reproductive Tract Recrudescence in an Imposex-Susceptible Mollusc

Abstract

The biocide tributyltin (TBT) causes the development of male sex characteristics in females of some molluscan species, a phenomenon known as imposex. Recent evidence suggests that the retinoid X receptor (RXR) participates in TBT-induced imposex. Accordingly, we hypothesized that RXR may contribute to the seasonal development of the male reproductive tract in molluscs and would be expressed in concert with this phenomenon. RXR was cloned and sequenced from an imposex-susceptble species, the eastern mud snail Ilyanassa obsoleta. The DNA-binding domain of the receptor protein was 100 and 97% identical to those of the rock shell Thais clavigera and the freshwater snail Biomphalaria glabrata. The ligand-binding domain was 93 and 92% identicalto the LBD of these two molluscan species, respectively. Phylogenetic analyses revealed that RXR is an ancient nuclear receptor whose origin predates the emergence of the Bilateria. Interestingly, though inexplicably, the molluscan RXRs were more similar to sequences of vertebrate RXRs than to the RXRs of other lophotrochozoan invertebrates. Next, the expression of RXR mRNA levels in the reproductive tract was determined through the reproductive cycle. RXR mRNA levels increased commensurate with reproductive tract recrudescence in both sexes. However, the timing of coordinate recrudescence-RXR expression differed between sexes. Results demonstrate that RXR expression is associated with reproductive tract recrudescence in both sexes; although, the timing of recrudescence may dictate sex-specific development. Retinoid signaling initiated by TBT during an inappropriate time in females may result in imposex.