Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-04-09
Page range: 331–353
Abstract views: 174
PDF downloaded: 10

Mitogenome of Alaudala cheleensis (Passeriformes: Alaudidae) and comparative analyses of Sylvioidea mitogenomes

College of Life Sciences, Shaanxi Normal University, Xi’an 710062, China Shaanxi Institute of Zoology, Xi’an 710032, China
School of Biological Sciences and Engineering, Shaanxi University of Technology, Hanzhong 723001, China
Shaanxi Institute of Zoology, Xi’an 710032, China
College of Life Sciences, Shaanxi Normal University, Xi’an 710062, China
College of Life Sciences, Shaanxi Normal University, Xi’an 710062, China
Shaanxi Institute of Zoology, Xi’an 710032, China
Aves Alaudala cheleensis Alaudidae Sylvioidea mitogenome comparative mitogenomic analysis phylogeny

Abstract

To gain a better understanding of mitogenome features and phylogenetic relationships in Sylvioidea, a superfamily of Passerida, suborder Passeri, Passeriformes, the whole mitogenome of Alaudala cheleensis Swinhoe (Alaudidae) was sequenced, a comparative mitogenomic analysis of 18 Sylvioidea species was carried out, and finally, a phylogeny was reconstructed based on the mitochondrial dataset. Gene order of the A. cheleensis mitogenome was similar to that of other Sylvioidea species, including the gene rearrangement of cytb-trnT-CR1-trnP-nad6-trnE-remnant CR2-trnF-rrnS. There was slightly higher A+T content than that of G+C in the mitogenome, with an obvious C skew. The ATG codon initiated all protein-coding genes, while six terminating codons were used. The secondary structure of rrnS contained three domains and 47 helices, whereas rrnL included six domains and 60 helices. All tRNAs could be folded into a classic clover-leaf secondary structure except for trnS (AGY). The CR1 could be divided into three domains, including several conserved boxes (C-string, F, E, D, C and B-box, Bird similarity box, CSB1). Comparative analyses within Sylvioidea mitogenomes showed that most mitochondrial features were consistent with that of the A. cheleensis mitogenome. The basal position of the Alaudidae within the Sylvioidea in our phylogenetic analyses is consistent with other recent studies.

 

References

  1. Aleix-Mata, G., Ruiz-Ruano, F.J., Pérez, J.M., Sarasa, M. & Sánchez, A. (2019) Complete mitochondrial genome of the Western Capercaillie Tetrao urogallus (Phasianidae, Tetraoninae). Zootaxa, 4550 (4), 585–593.

    https://doi.org/10.11646/zootaxa.4550.4.9

    Alström, P., Ericson, P.G.P., Olsson, U. & Sundberg, P. (2006) Phylogeny and classification of the avian superfamily Sylvioidea. Molecular Phylogenetics and Evolution, 38, 381–397.

    https://doi.org/10.1016/j.ympev.2005.05.015

    Alström, P., Olsson, U. & Lei, F.M. (2013) A review of the recent advances in the systematics of the avian superfamily Sylvioidea. Chinese Birds, 4, 99–131.

    https://doi.org/10.5122/cbirds.2013.0016

    Alström, P., van Linschooten, J., Donald, P.F., Sundev, G., Mohammadi, Z., Ghorbani, F., Shafaeipour, A., van den Berg, A., Robb, M., Aliabadian, M., Wei, C., Lei, F., Oxelman, B. & Olsson, U. (2021) Multiple species delimitation approaches applied to the avian lark genus Alaudala. Molecular Phylogenetics and Evolution, 154, 106994.

    https://doi.org/10.1016/j.ympev.2020.106994

    Baker, A.J. & Marshall, H.D. (1997) Mitochondrial control region sequences as tools for understanding evolution. In: Mindell, D.P. (Ed.), Avian Molecular Evolution and Systematics. Academic Press, San Diego, pp. 51–82.

    https://doi.org/10.1016/B978-012498315-1/50005-4

    Bensch, S. & Härlid, A. (2000) Mitochondrial genomic rearrangements in songbirds. Molecular Biology and Evolution, 17 (1), 107–113.

    https://doi.org/10.1093/oxfordjournals.molbev.a026223

    Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27, 573–580.

    https://doi.org/10.1093/nar/27.2.573

    Boore, J.L. (1999) Animal mitochondrial genomes. Nucleic Acids Research, 27 (8), 1767‒1780.

    https://doi.org/10.1093/nar/27.8.1767

    Brown, G.G., Gadaleta, G., Pepe, G., Saccone, C. & Sbisà, E. (1986) Structural conservation and variation in the D-loop-containing region of vertebrate mitochondrial DNA. Journal of Molecular Biology, 192, 503–511.

    https://doi.org/10.1016/0022-2836(86)90272-x

    Brown, W.M., George, M. & Wilson, A.C. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America, 76, 1967–1971.

    https://doi.org/10.1073/pnas.76.4.1967

    Cai, T., Cibois, A., Alström, P., Moyle, R.G., Kennedy, J.D., Shao, S., Zhang, R., Irestedt, M., Ericson, P.G.P., Gelang, M., Qu, Y., Lei, F. & Fjeldså, J. (2019) Near-complete phylogeny and taxonomic revision of the world’s babblers (Aves: Passeriformes). Molecular Phylogenetics and Evolution, 130, 346–356.

    https://doi.org/10.1016/j.ympev.2018.10.010

    Caparroz, R., Rocha, A.V., Cabanne, G.S., Tubaro, P., Aleixo, A., Lemmon, E.M. & Lemmon, A.R. (2018) Mitogenomes of two neotropical bird species and the multiple independent origin of mitochondrial gene orders in Passeriformes. Molecular Biology Reports, 45 (3), 279–285.

    https://doi.org/10.1007/s11033-018-4160-5

    Cerasale, D.J., Dor, R., Winkler, D.W. & Lovette, I.J. (2012) Phylogeny of the Tachycineta genus of New World swallows: insights from complete mitochondrial genomes. Molecular Phylogenetics and Evolution, 63 (1), 64–71.

    https://doi.org/10.1016/j.ympev.2011.12.014

    Clayton, D.A. (1991) Replication and transcription of vertebrate mitochondrial DNA. Annual Review Cell and Developmental Biology, 7, 453–478.

    https://doi.org/10.1146/annurev.cb.07.110191.002321

    Delport, W., Ferguson, J.W. & Bloomer, P. (2002) Characterization and evolution of the mitochondrial DNA control region in hornbills (Bucerotiformes). Journal of Molecular Evolution, 54 (6), 794–806.

    https://doi.org/10.1007/s00239-001-0083-0

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    https://doi.org/10.1093/nar/gkh340

    Fregin, S., Haase, M., Olsson, U. & Alström, P. (2012) New insights into family relationships within the avian superfamily Sylvioidea (Passeriformes) based on seven molecular markers. BMC Evolutionary Biology, 12, 157.

    https://doi.org/10.1186/1471-2148-12-157

    Gao, R.R., Huang, Y. & Lei, F.M. (2013) Sequencing and analysis of the complete mitochondrial genome of Remiz consobrinus. Zoological Research, 34, 228–237.

    doi: 10.11813/j.issn.0254-5853.2013.3.0228

    Ghorbani, F., Aliabadian, M., Zhang, R., Irestedt, M., Hao, Y., Sundev, G., Lei, F., Ma, M., Olsson, U. & Alström, P. (2020) Densely sampled phylogenetic analyses of the Lesser Short-toed Lark (Alaudala rufescens)-Sand Lark (A. raytal) species complex (Aves, Passeriformes) reveal cryptic diversity. Zoologica Scripta, 49, 427–439.

    https://doi.org/10.1111/zsc.12422

    Gibb, G.C., Kardailsky, O., Kimball, R.T., Braun, E.L. & Penny, D. (2007) Mitochondrial genomes and avian phylogeny: complex characters and resolvability without explosive radiations. Molecular Biology and Evolution, 24 (1), 269–280.

    https://doi.org/10.1093/molbev/msl158

    Gibb, G.C., England, R., Hartig, G., McLenachan, P.A., Taylor Smith, B.L., McComish, B.J., Cooper, A. & Penny, D. (2015) New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene. Genome Biology and Evolution, 7 (11), 2983–2995.

    https://doi.org/10.1093/gbe/evv196

    Gill, F., Donsker, D. & Rasmussen, P. (Eds.) (2020) IOC World Bird List (v 10.2). Available from: http://www.worldbirdnames.org/ (accessed 12 February 2021)

    Gong, J., Zhao, R.P., Huang, Q.R., Sun, X.M., Huang, L. & Jing, M.D. (2017) Two mitogenomes in Gruiformes (Amaurornis akool/A. phoenicurus) and the phylogenetic placement of Rallidae. Genes & Genomics, 39, 987‒995.

    https://doi.org/10.1007/s13258-017-0562-3

    Grant, J.R. & Stothard, P. (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Research, 36, W181‒W184.

    https://doi.org/10.1093/nar/gkn179

    Hahn, C., Bachmann, L. & Chevreux, B. (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—A baiting and iterative mapping approach. Nucleic Acids Research, 41, e129.

    https://doi.org/10.1093/nar/gkt371

    Huang, Z. & Ke, D. (2016) Structure and evolution of the Phasianidae mitochondrial DNA control region. Mitochondrial DNA Part A DNA Mapping Sequencing & Analysis, 27 (1), 350–354.

    https://doi.org/10.3109/19401736.2014.895987

    Huang, Z., Shen, Y. & Ma, Y. (2017) Structure and variation of the Fringillidae (Aves: Passeriformes) mitochondrial DNA control region and their phylogenetic relationship. Mitochondrial DNA Part A DNA Mapping Sequencing & Analysis, 28 (6), 867–871.

    https://doi.org/10.1080/24701394.2016.1199023

    Jiang, L., Chen, J., Wang, P., Ren, Q., Yuan, J., Qian, C., Hua, X., Guo, Z., Zhang, L., Yang, J., Wang, Y., Zhang, Q., Ding, H., Bi, D., Zhang, Z., Wang, Q., Chen, D. & Kan, X. (2015) The mitochondrial genomes of Aquila fasciata and Buteo lagopus (Aves, Accipitriformes): Sequence, structure and phylogenetic analyses. PLoS One, 10 (8), e0136297.

    https://doi.org/10.1371/journal.pone.0136297

    Kan, X.Z., Li, X.F., Zhang, L.Q., Chen, L., Qian, C.J., Zhang, X.W. & Wang, L. (2010) Characterization of the complete mitochondrial genome of the Rock Pigeon, Columba livia (Columbiformes: Columbidae). Genetics and Molecular Research, 9, 1234–1249.

    https://doi.org/10.4238/vol9-2gmr853

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Kück, P., Meid, S.A., Groß, C., Wägele, J.W. & Misof, B. (2014) AliGROOVE—visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support. BMC Bioinformatics, 15, 294.

    https://doi.org/10.1186/1471-2105-15-294

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870.

    https://doi.org/10.1093/molbev/msw054

    Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analysis. Molecular Biology and Evolution, 29, 1695–1701.

    https://doi.org/10.1093/molbev/mss020

    Lansman, R.A., Avise, J.C. & Huettel, M.D. (1983) Critical experimental test of the possibility of ‘paternal leakage’ of mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America, 80, 1969–1971.

    https://doi.org/10.1073/pnas.80.7.1969

    Lavrov, D.V., Brown, W.M. & Boore, J.L. (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proceedings of the National Academy of Sciences of the United States of America, 97, 13738–13742.

    https://doi.org/10.1073/pnas.250402997

    Li, X., Lin, L., Cui, A., Bai, J., Wang, X., Xin, C., Zhang, Z., Yang, C., Gao, R., Huang, Y. & Lei, F. (2016) Taxonomic status and phylogenetic relationship of tits based on mitogenomes and nuclear segments. Molecular Phylogenetics and Evolution, 104, 14–20.

    https://doi.org/10.1016/j.ympev.2016.07.022

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

    https://doi.org/10.1093/bioinformatics/btp187

    Lowe, T.M. & Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25, 955–964.

    https://doi.org/10.1093/nar/25.5.0955

    Ma, Y.G., Huang, Y. & Lei, F.M. (2014) Sequencing and phylogenetic analysis of the Pyrgilauda ruficollis (Aves, Passeridae) complete mitochondrial genome. Zoological Research, 35, 81–91.

    https://doi.org/10.11813/j.issn.0254-5853.2014.2.081

    Mackiewicz, P., Urantówka, A.D., Kroczak, A. & Mackiewicz, D. (2019) Resolving phylogenetic relationships within Passeriformes based on mitochondrial genes and inferring the evolution of their mitogenomes in terms of duplications. Genome Biology and Evolution, 11 (10), 2824–2849.

    https://doi.org/10.1093/gbe/evz209

    Manuel, L.L., Fonseca, M.M., Aldridge, D.C., Bogan, A.E., Gan, H.M., Ghamizi, M., Sousa, R., Teixeira, A., Varandas, S., Zanatta, D., Zieritz, A. & Froufe, E. (2017) The first Margaritiferidae male (M-type) mitogenome: mitochondrial gene order as a potential character for determining higher-order phylogeny within Unionida (Bivalvia). Journal of Molluscan Studies, 83, 249–252.

    https://doi.org/10.1093/mollus/eyx009

    Marshall, H.D. & Baker, A.J. (1997) Structural conservation and variation in the mitochondrial control region of fringilline finches (Fringilla spp.) and the greenfinch (Carduelis chloris). Molecular Biology and Evolution, 14, 173–184.

    https://doi.org/10.1093/oxfordjournals.molbev.a025750

    Mindell, D.P., Sorenson, M.D. & Dimcheff, D.E. (1998) Multiple independent origins of mitochondrial gene order in birds. Proceedings of the National Academy of Sciences of the United States of America, 95, 10693–10697.

    https://doi.org/10.1073/pnas.95.18.10693

    Pereira, S.L. (2000) Mitochondrial genome organization and vertebrate phylogenetics. Genetics and Molecular Biology, 23, 745–752.

    https://doi.org/10.1590/S1415-47572000000400008

    Perna, N.T. & Kocher, T.D. (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution, 41, 353–358.

    https://doi.org/10.1007/BF01215182

    Qian, C.J., Wang, Y.X., Guo, Z.C., Yang, J.K. & Kan, X.Z. (2013) Complete mitochondrial genome of skylark, Alauda arvensis (Aves: Passeriformes): The first representative of the family Alaudidae with two extensive heteroplasmic control regions. Mitochondrial DNA, 24, 246–248.

    https://doi.org/10.3109/19401736.2012.752481

    Rambaut, A., Suchard, M. & Drummond, A. (2004) Tracer. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 12 February 2021)

    Randi, E. & Lucchini, V. (1998) Organization and evolution of the mitochondrial DNA control region in the avian genus Alectoris. Journal of Molecular Evolution, 47 (4), 449–462.

    https://doi.org/10.1007/PL00006402

    Ritchie, P.A. & Lambert, D.M. (2000) A repeat complex in the mitochondrial control region of Adélie Penguins from Antarctica. Genome, 43 (4), 613–618.

    https://doi.org/10.1139/g00-018

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 9, 1572–1574.

    https://doi.org/10.1093/bioinformatics/btg180

    Ruokonen, M. & Kvist, L. (2002) Structure and evolution of the avian mitochondrial control region. Molecular Phylogenetics and Evolution, 23 (3), 422–432.

    https://doi.org/10.1016/s1055-7903(02)00021-0

    Saccone, C., Pesole, G. & Sbisá, E. (1991) The main regulatory region of mammalian mitochondrial DNA: Structure-function model and evolutionary pattern. Journal of Molecular Evolution, 33, 83‒91.

    https://doi.org/10.1007/BF02100199

    Sbisà, E., Tanzariello, F., Reyes, A., Pesole, G. & Saccone, C. (1997) Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene, 205, 125–140.

    https://doi.org/10.1016/s0378-1119(97)00404-6

    Sibley, C.G. & Ahlquist, J.E. (1990) Phylogeny and Classification of Birds: a Study in Molecular Evolution. Yale University Press, New Haven, xxiii+976 pp.

    https://doi.org/10.2307/j.ctt1xp3v3r

    Singh, T.R., Shneor, O. & Huchon, D. (2008) Bird mitochondrial gene order: insight from 3 warbler mitochondrial genomes. Molecular Biology and Evolution, 25, 475–477.

    https://doi.org/10.1093/molbev/msn003

    Skujina, I., McMahon, R., Lenis, V.P.E., Gkoutos, G.V. & Hegarty, M. (2016) Duplication of the mitochondrial control region is associated with increased longevity in birds. Aging, 8 (8), 1781–1789.

    https://doi.org/10.18632/aging.101012

    Song, X., Huang, J., Yan, C., Xu, G., Zhang, X. & Yue, B. (2015) The complete mitochondrial genome of Accipiter virgatus and evolutionary history of the pseudo-control regions in Falconiformes. Biochemical Systematics & Ecology, 58, 75–84.

    https://doi.org/10.1016/j.bse.2014.10.013

    Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    https://doi.org/10.1093/bioinformatics/btl446

    Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180.

    https://doi.org/10.1111/j.1096-0031.2010.00329.x

    Vali, Ü. (2002) Mitochondrial pseudo-control region in Old World eagles (genus Aquila). Molecular Ecology, 11, 2189–2194.

    https://doi.org/10.1046/j.1365-294x.2002.01578.x

    Wolstenholme, D.R. (1992) Animal mitochondrial DNA: structure and evolution. International Review of Cytology, 141, 173–216.

    https://doi.org/10.1016/S0074-7696(08)62066-5

    Yang, C., Lei, F.M. & Huang, Y. (2010) Sequencing and analysis of the complete mitochondrial genome of Pseudopodoces humilis (Aves, Paridae). Zoological Research, 31 (4), 333–344.

    https://doi.org/10.3724/SP.J.1141.2010.04333

    Yang, C., Yang, M., Wang, Q., Lu, Y. & Li, X. (2018) The complete mitogenome of Falco amurensis (Falconiformes, Falconidae), and a comparative analysis of genus Falco. Zoological Science, 35, 367–372.

    https://doi.org/10.2108/zs170182

    Zhou, X., Lin, Q., Fang, W. & Chen, X. (2014) The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements. BMC Genomics, 15, 573.

    https://doi.org/10.1186/1471-2164-15-573

    Zhong, Y., Zhou, M., Ouyang, B., Zeng, C., Zhang, M. & Yang, J. (2020) Complete mtDNA genome of Otus sunia (Aves, Strigidae) and the relaxation of selective constrains on Strigiformes mtDNA following evolution. Genomics, S0888-7543(19)31042-0. [Epub ahead of print]

    https://doi.org/10.1016/j.ygeno.2020.02.018.