Abstract
BackgroundThe Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. However, our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. Here we present a unique insight into the molecular pathways coordinating crustacean metamorphosis, by reconciling nuclear receptor (NR) gene activity from a 12-stage, 3-replicate transcriptome in the ornate spiny lobster (Panulirus ornatus) during larval development.ResultsWe annotated 18 distinct nuclear receptor genes, including three novel NRs which are upregulated prior to metamorphosis and have hence been named the “molt-associated receptors” (MARs). We also demonstrate the ecdysone-responsive expression of several known molt-related NRs including ecdysone receptor, fushi-tarazu-F1 and E75. Phylogenetic analysis of the curated NR family confirmed gene annotations and suggested that the MARs are a recent addition to the crustacean superfamily, occurring across the Malacostraca from the Stomatopoda to the Decapoda. The ligand-binding domain of these receptors appears to be less conserved than that of typical group-1 NRs. Expression data from two other crustacean species was utilized to examine MAR expression. The Y-organ of the tropical land crab showed a decline in expression of all MARs from intermolt to post-molt. Tissue distributions showed gonad-enriched expression in the Eastern rock lobster and antennal gland-enriched expression in the tropical land crab, although expression was evident across most tissues.ConclusionBy mining transcriptome data, we have curated an extensive list of NR genes expressed during the metamorphic molts of P. ornatus, including three novel crustacean NRs which appear to play a role in the molting process. Divergence of the E-region of these new receptors indicates that they may have adopted a function that is unconventional for NRs. Based on expression patterns, we can confirm that a number of NRs play a role in the ecdysone cassette which regulates molting in crustaceans. This study describes in detail the molecular events surrounding crustacean molting and metamorphosis by taking advantage of the distinctive life history unique to achelatan crustaceans.
Highlights
The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy
A subset of data was produced for principle component analysis (PCA) by filtering for emax > 3, which explained 23% of variance with the two upper principle components (PCs)
Here we report a comprehensive list of nuclear receptor (NR) found in an achelatan crustacean, whose unusual biology we have exploited to gain a high-resolution profile of gene expression during larval development
Summary
The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. Our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. We present a unique insight into the molecular pathways coordinating crustacean metamorphosis, by reconciling nuclear receptor (NR) gene activity from a 12-stage, 3-replicate transcriptome in the ornate spiny lobster (Panulirus ornatus) during larval development. Our understanding of molecular endocrinology in arthropods is quite well developed, with model insects lending an abundance of resources and knowledge to the field. Studies into developmental pathways are prolific, and subsequently the basis for insect metamorphosis has been well-examined over the past few decades. While many crustacean genes have been defined by conventional ortholog-hunting, their reconciliation with the endocrine pathways which they regulate is often dubious, and such inference is not always so insightful as one might optimistically expect
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