Genome-Wide Identification and Evolutionary Analysis of the ATP-Binding Cassette (ABC) Transporter Superfamily in Catfish

We recently assembled a large set of full-length transcripts by using RNA-Seq of a doubled-haploid catfish that has captured the majority of the catfish transcriptome. These full-length transcripts allowed analysis and annotation of gene families in catfish. In this work, we conducted a genome-wide search for and phylogenetic analysis of ATP-binding cassette (ABC) transporter gene superfamily. The ABC transporter genes encode membrane proteins that transport a diverse set of substrates across membranes, playing important roles in protecting organisms from xenobiotics. We identified 50 ABC transporters in catfish genome which were divided into seven subfamilies based on sequence similarities and phylogenetic relationships, including 9 ABCA genes, 12 ABCB genes, 12 ABCC genes, 5 ABCD genes, 2 ABCE genes, 4 ABCF genes and 6 ABCG genes. Most ABC transporters are conserved among vertebrates, though cases of recent gene duplications and gene losses do exist. By comparison with 48 human ABC transporter genes, ABCA subfamily has undergone the highest rate of gene duplication and loss during evolution. Seven of twelve human ABCA genes have catfish orthologous genes, while ABCA6, ABCA8, ABCA9, ABCA10 and ABCA13 were not present in the catfish genome, nor in several other sequenced fish genomes. All of these five genes in human are located in a single cluster together with ABCA5 on chromosome 17q24. This indicated that the expansion of the ABCA5-related gene cluster occurred after the split of lineages leading to tetrapods. Furthermore, ABCA1 and ABCA4 experienced fish-specific gene duplications. Ten of the eleven human ABCB genes have orthologs in catfish, with only ABCB1 being absent. The ABCB3 and ABCB6 are duplicated in catfish genome. There are twelve ABCC subfamily genes in human, eleven of which have orthologous genes in catfish, with ABCC11 being absent in catfish as well as in other sequenced fish genomes. All the four human ABCD transporters have orthologous genes in catfish, with ABCD4 experienced duplication in catfish. There are two copies of ABCE1 gene in catfish genome rather than one in human. All of the three human ABCF genes were found orthologs in catfish, with ABCF2 duplicated in catfish genome. The whole set of catfish ABC transporters provide the essential genomic resources for future biochemical, toxicological and physiological studies of ABC drug efflux transporters. The roles of ABC transporters experienced fish-specific expansion in catfish deserve more research on the adaptation to its specific living water environment. The characterization of ABC transporters in catfish genome, presented here, demonstrated the importance of full-length transcripts for comprehensive gene family annotation in catfish. On the other hand, all the catfish ABC transporter genes were fully supported by the phylogenetic trees, indicating the feasibility to construct phylogenetic trees for all catfish gene families that present the accurate evolutionary history as well as ortholog and paralog assignments.