Abstract
The mitochondrial genome can provide useful information for analyzing phylogeny and molecular evolution. In this study, the mitochondrial genome of Aphyocypris lini, an endangered and endemic minnow from southeast China, was sequenced and compared with other closely related species. The mitogenome of A. lini is 16,613 base pairs in length and consists of 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, two ribosomal RNA (rRNA) genes and one displacement loop region. All of PCGs initiate with the standard start codon ATG except cox1 with GTG and most PCGs terminate with TAA or TAG. The genome composition is highly A + T biased (57.3%), and exhibits a positive AT-skew (0.0614) and a negative GC-skew (−0.2205). Based on PCGs, phylogenetic analysis showed that former Ex-Danioninae subfamily was reclassified as Xenocyprididae and divided into two main clades: Opsariichthyinae and Xenocypridinae. Within Xenocypridinae, genus Aphyocypris is not monophyletic but closely related to Yaoshanicus, Nicholsicypris, and Pararasbora genera, suggesting taxonomy should be reconsidered. The present study contributes to understanding the comparative evolution and taxonomy of genus Aphyocypris.
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References
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693. https://doi.org/10.1093/nar/25.22.4692
Alves MJ, Coelho H, Collares-Pereira MJ, Coelho MM (2001) Mitochondrial DNA variation in the highly endangered cyprinid fish Anaecypris hispanica: importance for conservation. Heredity 87:463–473. https://doi.org/10.1046/j.1365-2540.2001.00929.x
Bachtrog D (2007) Reduced selection for codon usage Bias in Drosophila miranda. J Mol Evol 64:586–590. https://doi.org/10.1007/s00239-006-0257-x
Billington N, Hebert PD (1991) Mitochondrial DNA diversity in fishes and its implications for introductions. Can J Fish Aquat Sci 48:80–94. https://doi.org/10.1139/f91-306
Bozdogan H (1987) Model selection and Akaike's information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52:345–370. https://doi.org/10.1007/BF02294361
Chen Y (1998) China Fauna (Osteichthyes: Cpriniformes II). Science Press, Beijing, pp 171–175
Cooke SJ, Paukert C, Hogan Z (2012) Endangered river fish: factors hindering conservation and restoration. Endanger Species Res 17:179–191. https://doi.org/10.3354/esr00426
Du H, Chen X, Chen B (2003) Comparison and clarification between Nicholsicypris normalis and Yaoshanicus arcus. J South China Norm U 2:96–100 http://en.cnki.com.cn/Article_en/CJFDTOTAL-HNSF200302020.htm
Duchene S, Frey A, Alfaro-Núñez A, Dutton PH, Gilbert MTP, Morin PA (2012) Marine turtle mitogenome phylogenetics and evolution. Mol Phylogenet Evol 65:241–250. https://doi.org/10.1016/j.ympev.2012.06.010
Fang F (2003) Phylogenetic analysis of the Asian cyprinid genus Danio (Teleostei, Cyprinidae). Copeia 4:714–728. https://doi.org/10.2307/1448427
Fischer C, Koblmüller S, Gülly C, Schlötterer C, Sturmbauer C, Thallinger GG (2013) Complete mitochondrial DNA sequences of the threadfin cichlid (Petrochromis trewavasae) and the blunthead cichlid (Tropheus moorii) and patterns of mitochondrial genome evolution in cichlid fishes. PLoS One 8:e67048. https://doi.org/10.1371/journal.pone.0067048
Frazer-Abel AA, Hagerman PJ (2008) Core flexibility of a truncated metazoan mitochondrial tRNA. Nucleic Acids Res 36:5472–5481. https://doi.org/10.1093/nar/gkn529
Froese R, Pauly D (2019) FishBase. World Wide Web electronic publication. www.fishbase.org
Garey JR, Wolstenholme DR (1989) Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA ser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. J Mol Evol 28:374–387. https://doi.org/10.1007/BF02603072
George AL, Kuhajda BR, Williams JD, Cantrell MA, Rakes PL, Shute JR (2009) Guidelines for propagation and translocation for freshwater fish conservation. Fisheries 34:529–545. https://doi.org/10.1577/1548-8446-34.11.529
Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36:W181–W184. https://doi.org/10.1093/nar/gkn179
He S, Mayden RL, Wang X, Wang W, Tang KL, Chen WJ, Chen Y (2008) Molecular phylogenetics of the family Cyprinidae (Actinopterygii: Cypriniformes) as evidenced by sequence variation in the first intron of S7 ribosomal protein-coding gene: further evidence from a nuclear gene of the systematic chaos in the family. Mol Phylogen Evol 46:818–829. https://doi.org/10.1016/j.ympev.2007.06.001
Hu M, Wang Y, Cheung SG, Shin PKS, Xie Y (2009) Threatened fishes of the world: Aphyocypris lini Weitzman and Chan, 1966 (Cyprinidae). Environ Biol Fish 86:525–526. https://doi.org/10.1007/s10641-009-9560-x
Huang SP, Wang FY, Wang TY (2017) Molecular phylogeny of the Opsariichthys group (Teleostei: Cypriniformes) based on complete mitochondrial genomes. Zool Stud 56:e40. https://doi.org/10.6620/ZS.2017.56-40
Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y et al (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol Evol 30:2531–2540. https://doi.org/10.1093/molbev/mst141
Jiang Z, Jiang J, Wang Y, Zhang E, Zhang Y et al (2016) Red list of China’s vertebrates. Biodivers Sci 24:500–551. https://doi.org/10.17520/biods.2016076
Ko AM, Zhang Y, Yang MA, Hu Y, Cao P, Feng X, Zhang L, Wei F, Fu Q (2018) Mitochondrial genome of a 22,000-year-old giant panda from southern China reveals a new panda lineage. Curr Biol 28:R693–R694. https://doi.org/10.1016/j.cub.2018.05.008
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29(6):1695–1701. https://doi.org/10.1093/molbev/mss020
Letunic I, Bork P (2019) Interactive tree of life (itol) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259. https://doi.org/10.1093/nar/gkz239
Liao TY, Ünlü E, Kullander SO (2011a) Western boundary of the subfamily Danioninae in Asia (Teleostei, Cyprinidae): derived from the systematic position of Barilius mesopotamicus based on molecular and morphological data. Zootaxa 2880:31–40. https://doi.org/10.1186/1742-9994-8-12
Liao TY, Ünlü E, Kullander SO, Fang F (2011b) Phylogenetic position of rasborin cyprinids and monophyly of major lineages amongthe Danioninae, based on morphological characters (Cypriniformes: Cyprinidae). J Zool Syst Evol Res 49:224–232. https://doi.org/10.1111/j.1439-0469.2011.00621.x
Liao TY, Kullander SO, Lin HD (2011c) Synonymization of Pararasbora, Yaoshanicus, and Nicholsicypris with Aphyocypris, and description of a new species of Aphyocypris from Taiwan (Teleostei: Cyprinidae). Zool Stud 50:657–664 http://zoolstud.sinica.edu.tw/Journals/50.5/657.html
Liao TY, Kullander SO (2013) Phylogenetic significance of the kinethmoid-associated Y-shaped ligament and long intercostal ligaments in the Cypriniformes (Actinopterygii: Ostariophysi). Zool Scr 42:71–87. https://doi.org/10.1111/j.1463-6409.2012.00565.x
Liaw NHJ, Tsai CL, Watanabe K (2013) Complete mitochondrial genome of the Kikuchi's minnow Aphyocypris kikuchii (Teleostei, Cyprinidae). Mitochondrial DNA 24:11–13. https://doi.org/10.3109/19401736.2012.710227
Lowe TM, Chan PP (2016) tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucl Acids Res 44:W54–W57. https://doi.org/10.1093/nar/gkw413
Luo F, Luo T, Huang J, Liu X, Ling S, Wen Y (2019) Characterization of complete mitochondrial genome of Aphyocypris pulchrilineata (Teleostei, Cypriniformes, Cyprinidae). Mitochondrial DNA B 4:1267–1268. https://doi.org/10.1080/23802359.2019.1591221
Maitland PS (1995) The conservation of freshwater fish: past and present experience. Biol Conserv 72:259–270. https://doi.org/10.1016/0006-3207(94)00088-8
Mayden RL, Tang KT, Wood RM, Chen WJ, Agnew MK et al (2008) Inferring the tree of life of the order Cypriniformes, the earth’s most diverse clade of freshwater fishes: implications of varied taxon and character sampling. J Syst Evol 46:424–438 https://www.jse.ac.cn/EN/10.3724/SP.J.1002.2008.08062
Mayden RL, Chen WJ, Bart HL, Doosey MH, Simons AM et al (2009) Reconstructing the phylogenetic relationships of the earth’s most diverse clade of freshwater fishes-order Cypriniformes (Actinopterygii: Ostariophysi): a case study using multiple nuclear loci and the mitochondrial genome. Mol Phylogen Evol 51:500–514. https://doi.org/10.1016/j.ympev.2008.12.015
Nichols JT, Pope CH (1927) The fish of Hainan. Bull Amer Mus Hist 54:376 (http://biostor.org/reference/20650)
Nichols JT (1943) The fresh-water fishes of China. Nat Hist Central Asia 9:85–130. https://doi.org/10.5962/BHL.TITLE.12103
Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358. https://doi.org/10.1007/BF00186547
Ronquist F, Teslenko M, Mark PVD, Ayres DL, Darling A et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Satoh TP, Miya M, Mabuchi K, Nishida N (2016) Structure and variation of the mitochondrial genome of fishes. BMC Genomics 17:719. https://doi.org/10.1186/s12864-016-3054-y
Schönhuth S, Vukić J, Šanda R, Yang L, Mayden RL (2018) Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei). Mol Phylogen Evol 127:781–799. https://doi.org/10.1016/j.ympev.2018.06.026
Stout CC, Tan M, Lemmon AR, Lemmon EM, Armbruster JW (2016) Resolving Cypriniformes relationships using an anchored enrichment approach. BMC Evol Biol 16:1–13. https://doi.org/10.1186/s12862-016-0819-5
Sitoh K, Sado T, Mayden RL, Hanzawa N, Nakamura K et al (2006) Mitogenomic evolution and interrelationships of the Cypriniformes (Actinopterygii: Ostariophysi): the first evidence toward resolution of higher-level relationships of the world’s largest freshwater fish clade based on 59 whole mitogenome sequences. J Mol Evol 63:826–841. https://doi.org/10.1007/s00239-005-0293-y
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Tan M, Armbruster JW (2018) Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa 4476:6–39. https://doi.org/10.11646/zootaxa.4476.1.4
Tang KL, Agnew MK, Hirt MV, Sado T, Schneider LM et al (2010) Systematics of the subfamily Danioninae (Teleostei: Cypriniformes: Cyprinidae). Mol Phylogen Evol 57:189–214. https://doi.org/10.1016/j.ympev.2010.05.021
Tang B, Liu Y, Xin Z, Zhang D, Wang Z et al (2017) Characterisation of the complete mitochondrial genome of Helice wuana (Grapsoidea: Varunidae) and comparison with other brachyuran crabs. Genomics 110:221–230. https://doi.org/10.1016/j.ygeno.2017.10.001
Tao W, Mayden RL, He S (2013) Remarkable phylogenetic resolution of the most complex clade of Cyprinidae (Teleostei: Cypriniformes): a proof of concept of homology assessment and partitioning sequence data integrated with mixed model Bayesian analyses. Mol Phylogen Evol 66:603–616. https://doi.org/10.1016/j.ympev.2012.09.024
Vrijenhoek RC (1998) Conservation genetics of freshwater fish. J Fish Biol 53:394–412. https://doi.org/10.1111/j.1095-8649.1998.tb01039.x
Wang X, Li J, He S (2007) Molecular evidence for the monophyly of east Asian groups of Cyprinidae (Teleostei: Cypriniformes) derived from the nuclear recombination activating gene 2 sequences. Mol Phylogen Evol 42:157–170. https://doi.org/10.1016/j.ympev.2006.06.014
Wang Y, Shen Y, Feng C, Zhao K, Song Z, Zhang Y, Yang L, He S (2016) Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Sci Rep 6:29690. https://doi.org/10.1038/srep29690
Watanabe YL, Suematsu T, Ohtsuki T (2014) Losing the stem-loop structure from metazoan mitochondrial tRNAs and co-evolution of interacting factors. Front Genet 5:109. https://doi.org/10.3389/fgene.2014.00109
Weitzman SH, Chan LL (1966) Identification and relationships of Tanichthys albonubes and Aphyocypris pooni, two cyprinid fishes from South China and Hong Kong. Copeia 2:285–296. https://doi.org/10.2307/1441136
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. https://doi.org/10.1186/1471-2105-13-134
Yu P, Zhou L, Zhou XY, Yang WT, Zhang J (2019) Unusual AT-skew of Sinorhodeus microlepis mitogenome provides new insights into mitogenome features and phylogenetic implications of bitterling fishes. Int J Biol Macromol 129:339–350. https://doi.org/10.1016/j.ijbiomac.2019.01.200
Yue P, Chen Y (1998) Pisces. In: Wang S (ed) China red data book of endangered animals. Science Press, Beijing, pp 71–73
Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 20(1):348–355. https://doi.org/10.1111/1755-0998.13096
Zhang F, Shen Y (2019) Characterization of the complete mitochondrial genome of Rhinogobius leavelli (Perciformes: Gobiidae: Gobionellinae) and its phylogenetic analysis for Gobionellinae. Biologia 74:493–499. https://doi.org/10.2478/s11756-018-00189-5
Zhu X, Guo Y, Ma G, Long J (2015) A review of research progress on the genus Aphyocypris. J Kaili U 33:84–87. https://doi.org/10.3969/j.issn.1673-9329.2015.03.25
Zhu Y, Zhao Y, Huang K (2013) Aphyocypris pulchrilineata, a new miniature cyprinid species (Teleostei: Cypriniformes: Cyprinidae) from Guangxi, China. Ichthyol Res 60:232–236. https://doi.org/10.1007/s10228-013-0338-y
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We appreciate the journal editors and two anonymous reviewers for their constructive comments and suggestions on the manuscript. This research was supported by Fujian Middle-aged and Young Teacher Education Research Project (Grant No. JAT200445), the Science and Technology Program of Fuzhou, China (Grant No. 2019-S-64), and Fujian Fishery Structural Adjustment Special Fund subsidy Project (Grant No. 2020yyjg34).
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Zhang, Z., Li, S., Zhang, J. et al. The complete mitochondrial genome of an endangered minnow Aphyocypris lini (Cypriniformes: Xenocyprididae): genome characterization and phylogenetic consideration. Biologia 76, 3311–3321 (2021). https://doi.org/10.1007/s11756-021-00811-z
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DOI: https://doi.org/10.1007/s11756-021-00811-z