Abstract
BackgroundCell differentiation is mediated by synchronized waves of coordinated expression for hundreds to thousands of genes, and must be regulated to produce complex tissues and phenotypes. For many animal species, sexual selection has driven the development of elaborate male ornaments, requiring sex-specific differentiation pathways. One such male ornament is the pheromone-producing mental gland of the red-legged salamander (Plethodon shermani). Mental gland development follows an annual cycle of extreme hypertrophy, production of pheromones for the ~ 2 month mating season, and then complete resorption before repeating the process in the following year. At the peak of the mating season, the transcriptional and translational machinery of the mental gland are almost exclusively redirected to the synthesis of rapidly evolving pheromones. Of these pheromones, Plethodontid Modulating Factor (PMF) has experienced an unusual history: following gene duplication, the protein coding sequence diversified from positive sexual selection while the untranslated regions have been conserved by purifying selection. The molecular underpinnings that bridge the processes of gland hypertrophy, pheromone synthesis, and conservation of the untranslated regions remain to be determined.ResultsUsing Illumina sequencing, we prepared a de novo transcriptome of the mental gland at six stages of development. Differential expression analysis and immunohistochemistry revealed that the mental gland initially adopts a highly proliferative, almost tumor-like phenotype, followed by a rapid increase in pheromone mRNA and protein. One likely player in this transition is Cold Inducible RNA Binding Protein (CIRBP), which selectively and cooperatively binds the highly conserved PMF 3′ UTR. CIRBP, along with other proteins associated with stress response, have seemingly been co-opted to aid in mental gland development by helping to regulate pheromone synthesis.ConclusionsThe P. shermani mental gland utilizes a complex system of transcriptional and post-transcriptional gene regulation to facilitate its hypertrophication and pheromone synthesis. The data support the evolutionary interplay of coding and noncoding segments in rapid gene evolution, and necessitate the study of co-evolution between pheromone gene products and their transcriptional/translational regulators. Additionally, the mental gland could be a powerful emerging model of regulated tissue proliferation and subsequent resorption within the dermis and share molecular links to skin cancer biology.
Highlights
Cell differentiation is mediated by synchronized waves of coordinated expression for hundreds to thousands of genes, and must be regulated to produce complex tissues and phenotypes
Subsequent analysis by reverse-phase high performance liquid chromatography (RP-HPLC) revealed normal proportions of Plethodontid Receptivity Factor (PRF) and Plethodontid Modulating Factor (PMF), but with protein concentrations at ~ 33–50% of levels normally observed in mid-August
These data suggest that the mental gland initially forms as a tightly packed mass of cells with little cytoplasm, and upon induction of pheromone synthesis, cells swell with large volumes of pheromone, adopt a columnar shape, and the ECM condenses and/or degrades in order to support the enlarged cells
Summary
Cell differentiation is mediated by synchronized waves of coordinated expression for hundreds to thousands of genes, and must be regulated to produce complex tissues and phenotypes. In the marine gastropod abalone, males produce billions of sperm that overexpress the rapidly evolving protein lysin (up to ~ 1 g lysin per male abalone) that facilitates species-specific fertilization [14,15,16]; in fruit flies, male accessory glands synthesize complex mixtures of rapidly evolving seminal fluid proteins that restrict female re-mating by reducing her viability and survival [17, 18]; in Pieris butterflies, males produce enormous spermatophores (~ 13% of their body mass) that are encased in a nearly indestructible protein shell that slows spermatophore clearance and prevents female re-mating [19] In these examples, the molecular mechanisms underlying the regulated expression of these unusual reproductive proteins are not fully understood
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