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. 2016 Apr 8;11(4):e0153246.
doi: 10.1371/journal.pone.0153246. eCollection 2016.

Genome-Wide Identification, Characterization and Phylogenetic Analysis of ATP-Binding Cassette (ABC) Transporter Genes in Common Carp (Cyprinus carpio)

Xiang Liu  1   2 , Shangqi Li  1 , Wenzhu Peng  1 , Shuaisheng Feng  1 , Jianxin Feng  3 , Shahid Mahboob  4   5 , Khalid A Al-Ghanim  4 , Peng Xu  1   6
Affiliations

Genome-Wide Identification, Characterization and Phylogenetic Analysis of ATP-Binding Cassette (ABC) Transporter Genes in Common Carp (Cyprinus carpio)

Xiang Liu et al. PLoS One. .

Abstract

The ATP-binding cassette (ABC) gene family is considered to be one of the largest gene families in all forms of prokaryotic and eukaryotic life. Although the ABC transporter genes have been annotated in some species, detailed information about the ABC superfamily and the evolutionary characterization of ABC genes in common carp (Cyprinus carpio) are still unclear. In this research, we identified 61 ABC transporter genes in the common carp genome. Phylogenetic analysis revealed that they could be classified into seven subfamilies, namely 11 ABCAs, six ABCBs, 19 ABCCs, eight ABCDs, two ABCEs, four ABCFs, and 11 ABCGs. Comparative analysis of the ABC genes in seven vertebrate species including common carp, showed that at least 10 common carp genes were retained from the third round of whole genome duplication, while 12 duplicated ABC genes may have come from the fourth round of whole genome duplication. Gene losses were also observed for 14 ABC genes. Expression profiles of the 61 ABC genes in six common carp tissues (brain, heart, spleen, kidney, intestine, and gill) revealed extensive functional divergence among the ABC genes. Different copies of some genes had tissue-specific expression patterns, which may indicate some gene function specialization. This study provides essential genomic resources for future studies in common carp.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Phylogenetic tree of the ABC transporter family in seven species including common carp.
Neighbor-joining-based phylogenetic tree of ABC proteins sequences from seven vertebrate species: human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The ABC subfamilies are labeled from A–H.
Fig 2
Fig 2. Phylogenetic tree of the ABCA subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCA proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black dots indicate common carp genes.
Fig 3
Fig 3. Phylogenetic tree of ABCB subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCB proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black stars indicate common carp genes.
Fig 4
Fig 4. Phylogenetic tree of ABCC subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCC proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black dots indicate common carp genes.
Fig 5
Fig 5. Phylogenetic tree of ABCD subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCD proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black stars indicate common carp genes.
Fig 6
Fig 6. Phylogenetic tree of ABCE/F subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCE/F proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black dots indicate common carp genes.
Fig 7
Fig 7. Phylogenetic tree of ABCG/H subfamily transporters.
Neighbor-joining-based phylogenetic tree of ABCG/H proteins sequences. Human (Hsa), mouse (Mmu), chicken (Gga), frog (Xtr), medaka (Ola), zebrafish (Dre), and common carp (Cca). The black stars indicate common carp genes.
Fig 8
Fig 8. Conserved synteny blocks harboring the ABCG8 gene in vertebrate genomes.
Horizontal lines indicate orthologous relationships. Gene names: slc3a1 (solute carrier gene family 3, member 1); ppm1b (protein phosphatase, Mg2+/Mn2+ dependent, 1B); lrpprc (leucine-rich pentatricopeptide repeat containing); ABCG8 (ATP-binding cassette, sub-family G, member 8); ABCG5 (ATP-binding cassette, sub-family G, member 5); dync2li1 (dynein, cytoplasmic 2, light intermediate chain 1); pprc1 (peroxisome proliferator-activated receptor gamma coactivator-related protein 1).
Fig 9
Fig 9. Conserved synteny blocks harboring the ABCD3a gene in vertebrate genomes.
Horizontal lines indicate orthologous relationships. Gene names: nrp1a (neuropilin 1a); atp8a2 (ATPase, aminophospholipid transporter, class I, type 8A, member 2); GPR (G protein-coupled receptor); tmem56a (transmembrane protein 56a); f3a (coagulation factor IIIa); ABCD3a (ATP-binding cassette, sub-family D, member 3a); fam168b (family with sequence similarity 168, member B); CCDC (coiled-coil domain-containing protein).
Fig 10
Fig 10. Expression levels of common carp ABC transporter genes in six tissues by RT-PCR.
β-actin was used as an internal control. Gene names are indicated on the left of the panels. The six tissues are: BRA (brain), HEA (heart), SPL (spleen), KID (kidney), INT (intestine), and GIL (gill).
See this image and copyright information in PMC

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The authors acknowledge grant support from the National Natural Science Foundation of China (No.31422057), National High-Technology Research and Development Program of China (863 program; 2011AA100401), Special Scientific Research Funds for Central Non-profit Institutes of Chinese Academy of Fishery Sciences (2014A03YQ01; 2014C008) and Foundation of Beijing Key Laboratory of Fishery Biotechnology (201602). The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for funding this research (No. RG 1435-012).