The evolution of mitochondrial genomes in modern frogs (Neobatrachia): nonadaptive evolution of mitochondrial genome reorganization

BMC Genomics

Xiaomao Zeng²  Robert W Murphy³  Pamela BY Wong³  Ikuo Miura¹  Yuchi Zheng²  Yun Xia² 

[1] Insititute for Amphibian Biology, Graduate School of Science, Hiroshima University, Kagamiyama 1-3-1, Higashi-Hiroshima 739-8526, Japan;Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China;Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, Canada

关键词: Gene order;    Random gene loss;    Gene duplication;    Gene rearrangement;    tRNA gene;    Mitogenomics;   

Others  :  1216259
DOI  :  10.1186/1471-2164-15-691

 received in 2013-11-02, accepted in 2014-08-12,  发布年份 2014

【 摘 要 】

Background

Although mitochondrial (mt) gene order is highly conserved among vertebrates, widespread gene rearrangements occur in anurans, especially in neobatrachians. Protein coding genes in the mitogenome experience adaptive or purifying selection, yet the role that selection plays on genomic reorganization remains unclear. We sequence the mitogenomes of three species of Glandirana and hot spots of gene rearrangements of 20 frog species to investigate the diversity of mitogenomic reorganization in the Neobatrachia. By combing these data with other mitogenomes in GenBank, we evaluate if selective pressures or functional constraints act on mitogenomic reorganization in the Neobatrachia. We also look for correlations between tRNA positions and codon usage.

Results

Gene organization in Glandirana was typical of neobatrachian mitogenomes except for the presence of pseudogene trnS (AGY). Surveyed ranids largely exhibited gene arrangements typical of neobatrachian mtDNA although some gene rearrangements occurred. The correlation between codon usage and tRNA positions in neobatrachians was weak, and did not increase after identifying recurrent rearrangements as revealed by basal neobatrachians. Codon usage and tRNA positions were not significantly correlated when considering tRNA gene duplications or losses. Change in number of tRNA gene copies, which was driven by genomic reorganization, did not influence codon usage bias. Nucleotide substitution rates and d_N/d_S ratios were higher in neobatrachian mitogenomes than in archaeobatrachians, but the rates of mitogenomic reorganization and mt nucleotide diversity were not significantly correlated.

Conclusions

No evidence suggests that adaptive selection drove the reorganization of neobatrachian mitogenomes. In contrast, protein-coding genes that function in metabolism showed evidence for purifying selection, and some functional constraints appear to act on the organization of rRNA and tRNA genes. As important nonadaptive forces, genetic drift and mutation pressure may drive the fixation and evolution of mitogenomic reorganizations.

【 授权许可】

   
2014 Xia et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Boore JL: Animal mitochondrial genomes. Nucl Acids Res 1999, 27(8):1767-1780.
• [2]Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF: Characterization of 67 mitochondrial tRNA gene rearrangements in the hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol 2009, 26(7):1607-1617.
• [3]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.
• [4]Bernt M, Braband A, Schierwater B, Stadler PF: Genetic aspects of mitochondrial genome evolution. Mol Phylogenet Evol 2013, 69(2):328-338.
• [5]Das J: The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 2006, 28(9):890-901.
• [6]Galtier N, Nabholz B, Glemin S, Hurst G: Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 2009, 18(22):4541-4550.
• [7]Shen YY, Liang L, Zhu ZH, Zhou WP, Irwin DM, Zhang YP: Adaptive evolution of energy metabolism genes and the origin of flight in bats. Proc Natl Acad Sci USA 2010, 107(19):8666-8671.
• [8]Castoe T, De Koning A, Kim H, Gu W, Noonan B, Naylor G, Jiang Z, Parkinson C, Pollock D: Evidence for an ancient adaptive episode of convergent molecular evolution. Proc Natl Acad Sci USA 2009, 106(22):8986-8991.
• [9]Da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A: The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics 2008, 9:22.
• [10]Brown WM: The mitochondrial genome of animals. In Molecular evolutionary genetics. Edited by MacIntyre RJ. New York: Plenum Press; 1985:95-130.
• [11]Boussau B, Brown JM, Fujita MK: Nonadaptive evolution of mitochondrial genome size. Evolution 2011, 65(9):2706-2711.
• [12]Lynch M: The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci USA 2007, 104(Suppl 1):8597-8604.
• [13]Christianson T, Clayton D: A tridecamer DNA sequence supports human mitochondrial RNA 3'-end formation in vitro. Mol Cell Biol 1988, 8(10):4502-4509.
• [14]Satoh T, Sato Y, Masuyama N, Miya M, Nishida M: Transfer RNA gene arrangement and codon usage in vertebrate mitochondrial genomes: a new insight into gene order conservation. BMC Genomics 2010, 11(1):479.
• [15]Lavrov DV, Boore JL, Brown WM: Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Mol Biol Evol 2002, 19(2):163-169.
• [16]Gissi C, Iannelli F, Pesole G: Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 2008, 101(4):301-320.
• [17]Higgs PG, Ran WQ: Coevolution of codon usage and tRNA genes leads to alternative stable states of biased codon usage. Mol Biol Evol 2008, 25(11):2279-2291.
• [18]Duret L: tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet 2000, 16(7):287-289.
• [19]Rocha EPC: Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 2004, 14(11):2279-2286.
• [20]Schneider A: Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 2011, 80(1):1033-1053.
• [21]Xu W, Jameson D, Tang B, Higgs PG: The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol 2006, 63(3):375-392.
• [22]Kurabayashi A, Yoshikawa N, Sato N, Hayashi Y, Oumi S, Fujii T, Sumida M: Complete mitochondrial DNA sequence of the endangered frog Odorrana ishikawae (family Ranidae) and unexpected diversity of mt gene arrangements in ranids. Mol Phylogenet Evol 2010, 56(2):543-553.
• [23]Irisarri I, Mauro DS, Abascal F, Ohler A, Vences M, Zardoya R: The origin of modern frogs (Neobatrachia) was accompanied by acceleration in mitochondrial and nuclear substitution rates. BMC Genomics 2012, 13(1):626.
• [24]Zhang P, Liang D, Mao R-L, Hillis DM, Wake DB, Cannatella DC: Efficient sequencing of Anuran mtDNAs and a mitogenomic exploration of the phylogeny and evolution of frogs. Mol Biol Evol 2013, 30(8):1899-1915.
• [25]Roe BA, Ma DP, Wilson RK, Wong JFH: The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 1985, 260(17):9759-9774.
• [26]Pabijan M, Spolsky C, Uzzell T, Szymura JM: Comparative analysis of mitochondrial genomes in Bombina (Anura; Bombinatoridae). J Mol Evol 2008, 67(3):246-256.
• [27]Irisarri I, San Mauro D, Green D, Zardoya R: The complete mitochondrial genome of the relict frog Leiopelma archeyi: insights into the root of the frog Tree of Life. Mitochondrial DNA 2010, 21(5):173-182.
• [28]Alam M, Kurabayashi A, Hayashi Y, Sano N, Khan M, Fujii T, Sumida M: Complete mitochondrial genomes and novel gene rearrangements in two dicroglossid frogs, Hoplobatrachus tigerinus and Euphlyctis hexadactylus, from Bangladesh. Genes Genet Syst 2010, 85(3):219-232.
• [29]Sumida M, Kanamori Y, Kaneda H, Kato Y, Nishioka M, Hasegawa M, Yonekawa H: Complete nucleotide sequence and gene rearrangement of the mitochondria genome of the Japanese pond frog Rana nigromaculata. Genes Genet Syst 2001, 76(5):311-325.
• [30]Cao SY, Wu XB, Yan P, Hu YL, Su X, Jiang ZG: Complete nucleotide sequences and gene organization of mitochondrial genome of Bufo gargarizans. Mitochondrion 2006, 6(4):186-193.
• [31]Igawa T, Kurabayashi A, Usuki C, Fujii T, Sumida M: Complete mitochondrial genomes of three neobatrachian anurans: a case study of divergence time estimation using different data and calibration settings. Gene 2008, 407(1–2):116-129.
• [32]Su X, Wu XB, Yan P, Cao SY, Hu YL: Rearrangement of a mitochondrial tRNA gene of the concave-eared torrent frog, Amolops tormotus. Gene 2007, 394(1–2):25-34.
• [33]Ren ZM, Zhu B, Ma EB, Wen J, Tu TY, Cao Y, Hasegawa M, Zhong Y: Complete nucleotide sequence and gene arrangement of the mitochondrial genome of the crab-eating frog Fejervarya cancrivora and evolutionary implications. Gene 2009, 441(1–2):148-155.
• [34]Zhang JF, Nie LW, Wang Y, Hu LL: The complete mitochondrial genome of the large-headed frog, Limnonectes bannaensis (Amphibia: Anura), and a novel gene organization in the vertebrate mtDNA. Gene 2009, 442(1–2):119-127.
• [35]Zhou Y, Zhang JY, Zheng RQ, Yu BG, Yang G: Complete nucleotide sequence and gene organization of the mitochondrial genome of Paa spinosa (Anura: Ranoidae). Gene 2009, 447(2):86-96.
• [36]Shadel G, Clayton D: Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 1997, 66(1):409-435.
• [37]Kurabayashi A, Sumida M: Afrobatrachian mitochondrial genomes: genome reorganization, gene rearrangement mechanisms, and evolutionary trends of duplicated and rearranged genes. BMC Genomics 2013, 14(1):633.
• [38]Boore JL: The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In Comparative Genomics. Edited by Sankoff D, Nadeau J. Netherlands: Kluwer Academic Publishers, Springer; 2000:133-147.
• [39]San Mauro D, Gower DJ, Zardoya R, Wilkinson M: A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. Mol Biol Evol 2006, 23(1):227-234.
• [40]Mueller RL, Boore JL: Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Mol Biol Evol 2005, 22(10):2104-2112.
• [41]Kakehashi R, Kurabayashi A, Oumi S, Katsuren S, Hoso M, Sumida M: Mitochondrial genomes of Japanese Babina frogs (Ranidae, Anura): unique gene arrangements and the phylogenetic position of genus Babina. Genes Genet Syst 2013, 88(1):59-67.
• [42]Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sa RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC: The amphibian tree of life. Bull Amer Mus Nat Hist 2006, 297:1-370.
• [43]Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, Moriau L, Bossuyt F: Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA 2007, 104(3):887-892.
• [44]Roelants K, Bossuyt F: Archaeobatrachian paraphyly and pangaean diversification of crown-group frogs. Syst Biol 2005, 54(1):111-126.
• [45]Gissi C, San Mauro D, Pesole G, Zardoya R: Mitochondrial phylogeny of Anura (Amphibia): a case study of congruent phylogenetic reconstruction using amino acid and nucleotide characters. Gene 2006, 366(2):228-237.
• [46]Irisarri I, Vences M, San Mauro D, Glaw F, Zardoya R: Reversal to air-driven sound production revealed by a molecular phylogeny of tongueless frogs, family Pipidae. BMC Evol Biol 2011, 11(1):114.
• [47]Chen G, Wang B, Liu J, Xie F, Jiang J: Complete mitochondrial genome of Nanorana pleskei (Amphibia: Anura: Dicroglossidae) and evolutionary characteristics of the amphibian mitochondrial genomes. Curr Zool 2011, 57(6):785-805.
• [48]Alexander Pyron R, Wiens JJ: A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 2011, 61(2):543-583.
• [49]Stuart BL: The phylogenetic problem of Huia (Amphibia: Ranidae). Mol Phylogenet Evol 2008, 46(1):49-60.
• [50]Che J, Pang JF, Zhao H, Wu GF, Zhao EM, Zhang YP: Phylogeny of Raninae (Anura : Ranidae) inferred from mitochondrial and nuclear sequences. Mol Phylogenet Evol 2007, 43(1):1-13.
• [51]Dubois A: Notes on the classification of Ranidae (Amphibia, Anura). Bull Mensuel Soc Linn Lyon 1992, 61(10):305-352.
• [52]Boore JL, Brown WM: Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 1998, 8(6):668-674.
• [53]Boore JL: The use of genome-level characters for phylogenetic reconstruction. Trends Ecol Evol 2006, 21(8):439-446.
• [54]Boore JL, Fuerstenberg SI: Beyond linear sequence comparisons: the use of genome-level characters for phylogenetic reconstruction. Phil Trans R Soc B 2008, 363(1496):1445-1451.
• [55]Shan X, Xia Y, Zheng Y-C, Zou F-D, Zeng X-M: The complete mitochondrial genome of Quasipaa boulengeri (Anura: Dicroglossidae). Mitochondrial DNA 2014, 25(2):83-84.
• [56]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.
• [57]Kurabayashi A, Usuki C, Mikami N, Fujii T, Yonekawa H, Sumida M, Hasegawa M: Complete nucleotide sequence of the mitochondrial genome of a Malagasy poison frog Mantella madagascariensis: evolutionary implications on mitochondrial genomes of higher anuran groups. Mol Phylogenet Evol 2006, 39(1):223-236.
• [58]Macey JR, Schulte JA, Larson A, Papenfuss TJ: Tandem duplication via light-strand synthesis may provide a precursor for mitochondrial genomic rearrangement. Mol Biol Evol 1998, 15(1):71-75.
• [59]Jia WL, Higgs PG: Codon usage in mitochondrial genomes: distinguishing context-dependent mutation from translational selection. Mol Biol Evol 2008, 25(2):339-351.
• [60]Duchene AM, Pujol C, Marechal-Drouard L: Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 2009, 55(1):1-18.
• [61]Schneider A, Marechal-Drouard L: Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol 2000, 10(12):509-513.
• [62]Janke A, Xu XF, Arnason U: The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. Proc Natl Acad Sci USA 1997, 94(4):1276-1281.
• [63]Peng QL, Nie LW, Pu YG: Complete mitochondrial genome of Chinese big-headed turtle, Platysternon megacephalum, with a novel gene organization in vertebrate mtDNA. Gene 2006, 380(1):14-20.
• [64]Hoegg S, Vences M, Brinkmann H, Meyer A: Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Mol Biol Evol 2004, 21(7):1188-1200.
• [65]Meiklejohn CD, Montooth KL, Rand DM: Positive and negative selection on the mitochondrial genome. Trends Genet 2007, 23(6):259-263.
• [66]Castellana S, Vicario S, Saccone C: Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein–coding Genes. Genome Biol Evol 2011, 3:1067-1079.
• [67]Shao R, Dowton M, Murrell A, Barker SC: Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol 2003, 20(10):1612-1619.
• [68]Oliveira D, Raychoudhury R, Lavrov DV, Werren JH: Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol 2008, 25(10):2167-2180.
• [69]Chong RA, Mueller RL: Evolution along the mutation gradient in the dynamic mitochondrial genome of salamanders. Genome Biol Evol 2013, 5(9):1652-1660.
• [70]Ojala D, Montoya J, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. Nature 1981, 290(5806):470-474.
• [71]Lynch M, Koskella B, Schaack S: Mutation pressure and the evolution of organelle genomic architecture. Science 2006, 311(5768):1727-1730.
• [72]Sambrook J, Russell DW: Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Press; 2001.
• [73]Kurabayashi A, Sumida M: PCR primers for the neobatrachian mitochondrial genome. Curr Herpetol 2009, 28(1):1-11.
• [74]Lowe T, Eddy S: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 1997, 25(5):955-964.
• [75]Frost DR: Amphibian Species of the World: an online reference. Version 5.5 (31 January, 2011). 2011. [http://research.amnh.org/vz/herpetology/amphibia/ webcite]
• [76]Lupi R, Meo PDO, Picardi E, D’Antonio M, Paoletti D, Castrignanò T, Pesole G, Gissi C: MitoZoa: a curated mitochondrial genome database of metazoans for comparative genomics studies. Mitochondrion 2010, 10(2):192-199.
• [77]Xia X, Xie Z: DAMBE: Software package for data analysis in molecular biology and evolution. J Hered 2001, 92(4):371-373.
• [78]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [79]Kamatani T, Yamamoto T: Comparison of codon usage and tRNAs in mitochondrial genomes of Candida species. Biosystems 2007, 90:362-370.
• [80]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-552.
• [81]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25(11):1451-1452.
• [82]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
• [83]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25(7):1253-1256.
• [84]Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008, 57(5):758-771.
• [85]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755.
• [86]Cannone JJ, Subramanian S, Schnare MN, Collett JR, D'Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Müller KM: The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 2002, 3(1):2.