De Novo Assembly and Characterization of Two Transcriptomes Reveal Multiple Light-Mediated Functions in the Scallop Eye (Bivalvia: Pectinidae)

Abstract

BackgroundThe eye has evolved across 13 separate lineages of molluscs. Yet, there have been very few studies examining the molecular machinary underlying eye function of this group, which is due, in part, to a lack of genomic resources. The scallop (Bivalvia: Pectinidae) represents a compeling molluscan model to study photoreception due to its morphologically novel and separately evolved mirror-type eye. We sequenced the adult eye transcriptome of two scallop species to: 1) identify the phototransduction pathway components; 2) identify any additional light detection functions; and 3) test the hypothesis that molluscs possess genes not found in other animal lineages.ResultsA total of 3,039 contigs from the bay scallop, Argopecten irradians and 26,395 contigs from the sea scallop, Placopecten magellanicus were produced by 454 sequencing. Targeted BLAST searches and functional annotation using Gene Ontology (GO) terms and KEGG pathways identified transcripts from three light detection systems: two phototransduction pathways and the circadian clock, a previously unrecognized function of the scallop eye. By comparing the scallop transcriptomes to molluscan and non-molluscan genomes, we discovered that a large proportion of the transcripts (7,776 sequences) may be specific to the scallop lineage. Nearly one-third of these contain transmembrane protein domains, suggesting these unannotated transcripts may be sensory receptors.ConclusionsOur data provide the most comprehensive transcriptomic resource currently available from a single molluscan eye type. Candidate genes potentially involved in sensory reception were identified, and are worthy of further investigation. This resource, combined with recent phylogenetic and genomic data, provides a strong foundation for future investigations of the function and evolution of molluscan photosensory systems in this morphologically and taxonomically diverse phylum.

Transcriptome survey of phototransduction and clock genes in marine bivalves

“…The mantle of the scallop not only secretes biomineralization proteins along its edge to induce shell formation, but it is also responsible for light-mediated functions and circadian rhythms due to 30-200 single chambered eyes along the mantle edge (Parsons et al, 1992;Pairett and Serb, 2013). In the present study, comparison of the phototransduction and circadian clock genes among four bivalve species indicated that the lack of target genes in scallops of P. magellanicus and A. irradians may be due to the low read depth in their transcriptomes, which both have less than one million reads (114,052 reads for A. irradians and 654,002 reads for P. magellanicus) generated from only eye tissue.…”

“…The unigene with the lowest E-value was selected as the representative when several unique transcripts were assigned to the same reference gene. The identified phototransduction and circadian genes in P. yessoensis were compared to those within the oyster C. gigas and the scallops Placopecten magellanicus and Argopecten irradians, which were previously summarized by Pairett and Serb (2013) from the eye transcriptome.…”

“…The expression data for Placopecten magellanicus and Argopecten irradians are summarized from Pairett and Serb (2013). Data for gene expression in the mantle of Crassostrea gigas were downloaded from an online database (http://www.oysterdb.com/).…”

“…A number of molecular components involved in circadian rhythms have now been discovered, including the circadian locomotor output cycles kaput (clock), period (per), timeless (tim), and cryptochrome (cry; Wager-Smith and Kay, 2000;Golombek and Rosenstein, 2010;Pairett and Serb, 2013). However, the molecular understanding of circadian rhythms is almost exclusively related to terrestrial species.…”

“…As a high-throughput method for transcriptome sequencing, RNA-Seq has been widely applied to uncover genes central to the circadian clock at the transcriptome level (Vize, 2009;Pairett and Serb, 2013;Shoguchi et al, 2013). To explore the potential genes underlying biological rhythms in marine species and investigate how these genes are correlated with terrestrial models, we made use of the recent generation of a large expressed sequence tag (EST) dataset developed from the mantle transcriptomes of marine bivalves (Pairett and Serb, 2013;Sun et al, 2015). The analysis allowed us to identify most of the key circadian genes from insects and mammals in the transcriptomes of marine bivalves, which indicated that many of these genes are very highly conserved in the animal kingdom.…”