BMC Genomics | |
The complete mitochondrial genomes of sixteen ardeid birds revealing the evolutionary process of the gene rearrangements | |
Xiaolin Chen1  Wenzhen Fang1  Qingxian Lin1  Xiaoping Zhou1  | |
[1] Key Laboratory of Ministry of Education for Coast and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen 361102, People’s Republic of China | |
关键词: Ardeidae; Phylogeny; Concerted evolution; Gene rearrangement; Mitochondrial genome; | |
Others : 856569 DOI : 10.1186/1471-2164-15-573 |
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received in 2014-02-09, accepted in 2014-07-03, 发布年份 2014 | |
【 摘 要 】
Background
The animal mitochondrial genome is generally considered to be under selection for both compactness and gene order conservation. As more mitochondrial genomes are sequenced, mitochondrial duplications and gene rearrangements have been frequently identified among diverse animal groups. Although several mechanisms of gene rearrangement have been proposed thus far, more observational evidence from major taxa is needed to validate specific mechanisms. In the current study, the complete mitochondrial DNA of sixteen bird species from the family Ardeidae was sequenced and the evolution of mitochondrial gene rearrangements was investigated. The mitochondrial genomes were then used to review the phylogenies of these ardeid birds.
Results
The complete mitochondrial genome sequences of the sixteen ardeid birds exhibited four distinct mitochondrial gene orders in which two of them, named as “duplicate tRNAGlu–CR” and “duplicate tRNAThr–tRNAPro and CR”, were newly discovered. These gene rearrangements arose from an evolutionary process consistent with the tandem duplication - random loss model (TDRL). Additionally, duplications in these gene orders were near identical in nucleotide sequences within each individual, suggesting that they evolved in concert. Phylogenetic analyses of the sixteen ardeid species supported the idea that Ardea ibis, Ardea modesta and Ardea intermedia should be classified as genus Ardea, and Ixobrychus flavicollis as genus Ixobrychus, and indicated that within the subfamily Ardeinae, Nycticorax nycticorax is closely related to genus Egretta and that Ardeola bacchus and Butorides striatus are closely related to the genus Ardea.
Conclusions
The duplicate tRNAThr–CR gene order is found in most ardeid lineages, suggesting this gene order is the ancestral pattern within these birds and persisted in most lineages via concerted evolution. In two independent lineages, when the concerted evolution stopped in some subsections due to the accumulation of numerous substitutions and deletions, the duplicate tRNAThr–CR gene order was transformed into three other gene orders. The phylogenetic trees produced from concatenated rRNA and protein coding genes have high support values in most nodes, indicating that the mitochondrial genome sequences are promising markers for resolving the phylogenetic issues of ardeid birds when more taxa are added.
【 授权许可】
2014 Zhou et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140723033611708.pdf | 392KB | download | |
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【 图 表 】
【 参考文献 】
- [1]Desjardins P, Morais R: Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol 1990, 212(4):599-634.
- [2]Mindell DP, Sorenson MD, Dimcheff DE: Multiple independent origins of mitochondrial gene order in birds. Proc Natl Acad Sci U S A 1998, 95(18):10693-10697.
- [3]Bensch S, Harlid A: Mitochondrial genomic rearrangements in songbirds. Mol Biol Evol 2000, 17(1):107-113.
- [4]Haddrath O, Baker AJ: Complete mitochondrial DNA genome sequences of extinct birds: ratite phylogenetics and the vicariance biogeography hypothesis. Proc Biol Sci 2001, 268(1470):939-945.
- [5]Eberhard JR, Wright TF, Bermingham E: Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Mol Biol Evol 2001, 18(7):1330-1342.
- [6]Haring E, Kruckenhauser L, Gamauf A, Riesing MJ, Pinsker W: The complete sequence of the mitochondrial genome of Buteo buteo (Aves, Accipitridae) indicates an early split in the phylogeny of raptors. Mol Biol Evol 2001, 18(10):1892-1904.
- [7]Abbott CL, Double MC, Trueman JW, Robinson A, Cockburn A: An unusual source of apparent mitochondrial heteroplasmy: duplicate mitochondrial control regions in Thalassarche albatrosses. Mol Ecol 2005, 14(11):3605-3613.
- [8]Gibb GC, Kardailsky O, Kimball RT, Braun EL, Penny D: Mitochondrial genomes and avian phylogeny: complex characters and resolvability without explosive radiations. Mol Biol Evol 2007, 24(1):269-280.
- [9]Singh TR, Shneor O, Huchon D: Bird mitochondrial gene order: insight from 3 warbler mitochondrial genomes. Mol Biol Evol 2008, 25(3):475-477.
- [10]Cadahia L, Pinsker W, Negro JJ, Pavlicev M, Urios V, Haring E: Repeated sequence homogenization between the control and pseudo-control regions in the mitochondrial genomes of the subfamily Aquilinae. J Exp Zool B Mol Dev Evol 2009, 312B(3):171-185.
- [11]Cho HJ, Eda M, Nishida S, Yasukochi Y, Chong JR, Koike H: Tandem duplication of mitochondrial DNA in the black-faced spoonbill. Platalea minor Genes Genet Syst 2009, 84(4):297-305.
- [12]Eda M, Kuro-o M, Higuchi H, Hasegawa H, Koike H: Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidae (albatrosses). Genes Genet Syst 2010, 85(2):129-139.
- [13]Verkuil YI, Piersma T, Baker AJ: A novel mitochondrial gene order in shorebirds (Scolopacidae, Charadriiformes). Mol Phylogenet Evol 2010, 57(1):411-416.
- [14]Morris-Pocock JA, Taylor SA, Birt TP, Friesen VL: Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evol Biol 2010, 10:14.
- [15]Sammler S, Bleidorn C, Tiedemann R: Full mitochondrial genome sequences of two endemic Philippine hornbill species (Aves: Bucerotidae) provide evidence for pervasive mitochondrial DNA recombination. BMC Genomics 2011, 12:35.
- [16]Schirtzinger EE, Tavares ES, Gonzales LA, Eberhard JR, Miyaki CY, Sanchez JJ, Hernandez A, Mueller H, Graves GR, Fleischer RC, Wright TF: Multiple independent origins of mitochondrial control region duplications in the order Psittaciformes. Mol Phylogenet Evol 2012, 64(2):342-356.
- [17]Gibb GC, Kennedy M, Penny D: Beyond phylogeny: pelecaniform and ciconiiform birds, and long-term niche stability. Mol Phylogenet Evol 2013, 68(2):229-238.
- [18]Boore JL: The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In Computational biology series, vol.1. Edited by Sankoff D, Dordrecht NJ. Netherlands: Kluwer Academic Publishers; 2000:133-147.
- [19]Kumazawa Y, Ota H, Nishida M, Ozawa T: The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions. Genetics 1998, 150(1):313-329.
- [20]Kurabayashi A, Sumida M, Yonekawa H, Glaw F, Vences M, Hasegawa M: Phylogeny, recombination, and mechanisms of stepwise mitochondrial genome reorganization in mantellid frogs from Madagascar. Mol Biol Evol 2008, 25(5):874-891.
- [21]Kushlan JA, Hancock JA: Herons (Ardeidae) (Bird Families of the World). New York: Oxford University Press; 2005.
- [22]Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T: A phylogenomic study of birds reveals their evolutionary history. Science 2008, 320(5884):1763-1768.
- [23]Zhou X, Wang Y, Chen X, Lin Q, Fang W, Wei D: PERMANENT GENETIC RESOURCES: A set of primer pairs for amplifying the complete mitochondrial DNA of endangered Chinese egret (Aves, Ardeidae, Egretta eulophotes). Mol Ecol Resour 2008, 8(2):412-414.
- [24]Zhang L, Wang L, Gowda V, Wang M, Li X, Kan X: The mitochondrial genome of the Cinnamon Bittern, Ixobrychus cinnamomeus (Pelecaniformes: Ardeidae): sequence, structure and phylogenetic analysis. Mol Biol Rep 2012, 39(8):8315-8326.
- [25]Nishibori M, Hayashi T, Tsudzuki M, Yamamoto Y, Yasue H: Complete sequence of the Japanese quail (Coturnix japonica) mitochondrial genome and its genetic relationship with related species. Anim Genet 2001, 32(6):380-385.
- [26]Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP: Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 1999, 12(2):105-114.
- [27]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
- [28]Huang X, Miller W: A time-efficient, linear-space local similarity algorithm. Adv Appl Math 1991, 12(3):373-381.
- [29]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-552.
- [30]Lanfear R, Calcott B, Ho SY, Guindon S: Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 2012, 29(6):1695-1701.
- [31]Miller MA, Pfeiffer W, Schwartz T: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE): Nov 14, 2010. New Orleans, LA; 2010:1-8.
- [32]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
- [33]Stamatakis A: RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30(9):1312-1313.
- [34]Quinn TW, Wilson AC: Sequence evolution in and around the mitochondrial control region in birds. J Mol Evol 1993, 37(4):417-425.
- [35]Ramirez V, Savoie P, Morais R: Molecular characterization and evolution of a duck mitochondrial genome. J Mol Evol 1993, 37(3):296-310.
- [36]Ritchie PA, Lambert DM: A repeat complex in the mitochondrial control region of Adelie penguins from Antarctica. Genome 2000, 43(4):613-618.
- [37]Ruokonen M, Kvist L: Structure and evolution of the avian mitochondrial control region. Mol Phylogenet Evol 2002, 23(3):422-432.
- [38]Buehler DM, Baker AJ: Characterization of the red knot (Calidris canutus) mitochondrial control region. Genome 2003, 46(4):565-572.
- [39]Bock WJ: A generic review of the family Ardeidae (Aves). Am Mus Novit 1956, 1779:1-49.
- [40]McCracken KG, Sheldon FH: Avian vocalizations and phylogenetic signal. Proc Natl Acad Sci U S A 1997, 94(8):3833-3836.
- [41]Peters JL: Check-list of birds of the world, vol. 1. Cambridge, Massachusetts: Harvard University Press; 1931.
- [42]McCracken KG, Sheldon FH: Molecular and osteological heron phylogenies: sources of incongruence. Auk 1998, 115(1):127-141.
- [43]Payne RB, Risley CJ: Systematics and evolutionary relationships among the herons (Ardeidae). Misc Publ Mus Zool Univ Mich 1976, 150:1-115.
- [44]Sheldon FH: Phylogeny of herons estimated from DNA-DNA hybridization data. Auk 1987, 104(1):97-108.
- [45]Sheldon FH, Jones CE, McCracken KG: Relative patterns and rates of evolution in heron nuclear and mitochondrial DNA. Mol Biol Evol 2000, 17(3):437-450.
- [46]Bergsten J: A review of long‒branch attraction. Cladistics 2005, 21(2):163-193.
- [47]Shao R, Barker SC, Mitani H, Aoki Y, Fukunaga M: Evolution of duplicate control regions in the mitochondrial genomes of metazoa: a case study with Australasian Ixodes ticks. Mol Biol Evol 2005, 22(3):620-629.
- [48]Lee JS, Miya M, Lee YS, Kim CG, Park EH, Aoki Y, Nishida M: The complete DNA sequence of the mitochondrial genome of the self-fertilizing fish Rivulus marmoratus (Cyprinodontiformes, Rivulidae) and the first description of duplication of a control region in fish. Gene 2001, 280(1–2):1-7.
- [49]Tatarenkov A, Avise JC: Rapid concerted evolution in animal mitochondrial DNA. Proc Biol Sci 2007, 274(1619):1795-1798.
- [50]Sano N, Kurabayashi A, Fujii T, Yonekawa H, Sumida M: Complete nucleotide sequence of the mitochondrial genome of Schlegel’s tree frog Rhacophorus schlegelii (family Rhacophoridae): duplicated control regions and gene rearrangements. Genes Genet Syst 2005, 80(3):213-224.
- [51]Kumazawa Y, Ota H, Nishida M, Ozawa T: Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol Biol Evol 1996, 13(9):1242-1254.
- [52]Dong S, Kumazawa Y: Complete mitochondrial DNA sequences of six snakes: phylogenetic relationships and molecular evolution of genomic features. J Mol Evol 2005, 61(1):12-22.
- [53]Sammler S, Ketmaier V, Havenstein K, Tiedemann R: Intraspecific rearrangement of duplicated mitochondrial control regions in the Luzon Tarictic Hornbill Penelopides manillae (Aves: Bucerotidae). J Mol Evol 2013, 77(5–6):199-205.