Extreme primary and secondary protein structure variability in the chimeric male-transmitted cytochrome c oxidase subunit II protein in freshwater mussels: Evidence for an elevated amino acid substitution rate in the face of domain-specific purifying selection

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Chapman, Eric G ^a   Piontkivska, Helen ^a   Walker, Jennifer M ^b   Stewart, Donald T ^c   Curole, Jason P ^d   Hoeh, Walter R ^a  

^a KENT STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN MISSISSIPPI   (United States)

^c ACADIA UNIVERSITY   (Canada)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; CYTOCHROME C OXIDASE SUBUNIT II; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COX2 GENE; EVOLUTION; GENE; GENE DELETION; GENE INSERTION; GENETIC CONSERVATION; GENOME; HYDROPHILICITY; MUSSEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; ANIMAL; BIVALVE; CHIMERA; DNA SEQUENCE; ENZYMOLOGY; FEMALE; GENETIC SELECTION; GENETICS; INHERITANCE; MALE; MOLECULAR EVOLUTION;

ANIMALIA; BIVALVIA; METAZOA; MYTILOIDA; UNIONOIDEA; VENEROIDA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BIVALVIA; CHIMERA; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; FEMALE; INHERITANCE PATTERNS; MALE; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA;

EID: 47249144103     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-165     Document Type: Article

References (95)

1. Cytochrome c oxidase - structure, function, and physiology of a redox-driven molecular machine. O-MH Richter B Ludwig, Rev Physiol Biochem Pharmacol 2003 147 47 74 12783267
2. Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. J Castresana M Lübben M Saraste DG Higgins, EMBO J 1994 13 2516 2525 8013452
3. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. S Iwata C Ostermeier B Ludwig H Michel, Nature 1995 376 660 669 7651515
4. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å T Tsukhihara H Aoyama E Yamashita T Tomizaki H Yamaguchi K Shinzawa-Itoh R Nakashima R Yaono S Yoshikawa, Science 1996 272 1136 1144 8638158
5. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. R Nielsen Z Yang, Genetics 1998 148 929 936 9539414
6. Codon-substitution models for heterogeneous selection pressure at amino acid sites. ZH Yang R Nielsen R Goldman AMK Pedersen, Genetics 2000 155 431 449 10790415
7. Does nonneutral evolution shape observed patterns of DNA variation in animal mitochondrial genomes? AS Gerber R Loggins S Kumar TE Dowling, Annu Rev Genet 2001 35 539 566 11700293
8. The units of selection on mitochondrial DNA. DM Rand, Annu Rev Ecol Syst 2001 32 415 48
9. The incomplete natural history of mitochondria. JWO Ballard MC Whitlock, Molec Ecol 2004 13 729 744
10. Accelerated evolution of the electron transport chain in anthropoid primates. LI Grossman DE Wildman TR Schmidt M Goodman, TREE 2004 20 578 585
11. Molecular evolution of cytochrome c oxidase in high performance fish. AC Dalziel CD Moyes E Fredriksson SC Lougheed, J Mol Evol 2006 62 319 331 16477525
12. Molecular evolution at the cytochrome oxidase subunit 2 gene among divergent populations of the intertidal copepod, Tigriopus californicus. PD Rawson RS Burton, J Mol Evol 2006 62 753 764 16752213
13. Ancient sex-specific extension of the cytochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance. JP Curole TD Kocher, Mol Biol Evol 2002 19 1323 1328 12140244
14. Evolution of a unique mitotype-specific protein-coding extension of the cytochrome c oxidase II gene in freshwater mussels (Bivalvia: Unionoida). JP Curole TD Kocher, J Mol Evol 2005 61 381 389 16082567
15. Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). WR Hoeh DT Stewart B Sutherland E Zouros, Evolution 1996 50 2276 2286
16. High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in fresh water mussels (Bivalvia: Unionoidea). WR Hoeh DT Stewart SI Guttman, Evolution 2002 56 2252 2261 12487355
17. Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis. H-P Liu JB Mitton S-K Wu, Evolution 1996 50 952 957
18. An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca Bivalvia). M Passamonti, BMC Evol Biol 2007 7 Suppl 2 S7 17767735
19. Taxonomic distribution and phylogenetic utility of gender-associated mitochondrial genomes in the Unionoida (Bivalvia). JM Walker JP Curole DE Wade EG Chapman AE Bogan GT Watters WR Hoeh, Malacologia 2006 48 265 282
20. Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes phillippinarum (Mollusca: Bivalvia). M Passamonti V Scali, Curr Genet 2001 39 117 124 11405096
21. The unusual system of doubly uniparental inheritance of mtDNA: isn't one enough? S Breton HD Beaupré DT Stewart WH Hoeh PU Blier, Trends Genet 2007 23 465 474 17681397
22. The fate of paternal mitochondrial DNA in developing female mussels Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. B Sutherland D Stewart ER Kenchington E Zouros, Genetics 1998 148 341 347 9475744
23. Inheritance of two M type mitochondrial DNA from sperm and unfertilized eggs to offspring in Mytilus galloprovincialis. M Obata N Sano K Kawamura A Komaru, Develop Growth Differ 2007 49 335 344
24. Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. DOF Skibinski C Gallagher CM Beynon, Genetics 1994 138 801 809 7851776
25. Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. PD Rawson TJ Hilbish, Mol Biol Evol 1995 12 893 901 7476135
26. Male and female mitochondrial DNA lineages in the Blue mussel (Mytilus edulis) species group. DT Stewart C Saavedra RR Stanwood A Ball E Zouros, Mol Biol Evol 1995 12 735 747 7476121
27. Combining paternally and maternally inherited mitochondrial DNA for analysis of population structure in mussels. RA Krebs, Molec Ecol 2004 13 1701 1705
28. The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. A Mizi E Zouros N Moschonas GC Rodakis, Mol Biol Evol 2005 22 952 967 15647523
29. The evolution of the Unionacea in North America, and its implications for the worldwide fauna. GT Watters, Ecology and Evolution of the Freshwater Mussels (Unionoida) Berlin: Springer-Verlag, Bauer G, Wächtler K, 2001 281 307
30. Presence of a unique male-specific extension of C-terminus to the cytochrome c oxidase subunit II protein coded by the male-transmitted mitochondrial genome of Venustaconcha ellipsiformis (Bivalvia: Unionoidea). R Chakrabarti JM Walker DT Stewart RJ Trdan S Vijatraghavan J Curole WR Hoeh, FEBS Lett 2006 580 862 866 16414043
31. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman, Nucleic Acids Res 1997 25 3389 3402 http://ncbi.nlm.nih.gov/BLAST 9254694
32. Phylogeny of North American amblemines (Bivalvia, Unionoida): prodigious polyphyly proves pervasive across genera. DC Campbell JM Serb JE Buhay KJ Roe RL Minton C Lydeard, Invert Biol 2005 124 131 164
33. Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes. LS Jermiin D Graur RM Lowe RH Crozier, J Mol Evol 1994 39 160 173 7932780
34. Estimating the influence of selection on the variable amino acid sites of the cytochrome b protein functional domains. DA McClellan KG McCracken, Mol Biol Evol 2001 18 917 925 11371579
35. A re-evaluation of the recent Unionacea (Pelecypoda) of North America. WH Heard RH Guckert, Malacalogia 1970 10 333 335
36. The Etherioidea revisited: a phylogenetic analysis of hyriid relationships (Mollusca: Bivalvia: Paleoheterodonta: Unionoida). DL Graf, Occas Pap Mus Zool Univ Mich 2000 729 1 21
37. A phylogenetic perspective on the evolution of morphological and reproductive characteristics in the Unionoida. WR Hoeh AE Bogan WH Heard, Ecological studies, 145: Ecology and evolution of the freshwater mussels Unionoida Berlin: Springer-Verlag, Bauer G, Wächlter K, 2001 257 280
38. Systematics of freshwater mussels (Bivalvia: Unionoida). KJ Roe WR Hoeh, Molecular Systematics and Phylogeography of Mollusks Washington: Smithsonian Books, Lydeard C, Lindberg DR, 2003 91 122
39. Reproductive function for a c-terminus extended, male-transmitted cytochrome c oxidase subunit II protein expressed in both spermatozoa and eggs. R Chakrabarti JM Walker EG Chapman S Shepardson RJ Trdan JP Curole GT Watters DT Stewart S Vijatraghavan WR Hoeh, FEBS Lett 2007 581 5213 5219 17950289
40. Membrane-protein topology. G von Heijne, Nat Rev Mol Cell Biol 2006 7 909 918 17139331
41. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. AL Hughes M Nei, Nature 1988 335 167 170 3412472
42. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. AL Hughes M Nei, Proc Natl Acad Sci USA 1989 86 958 962 2492668
43. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. EC Metz SR Palumbi, Mol Biol Evol 1996 13 397 406 8587504
44. Patterns of nucleotide substitution in pseudogenes and functional genes. T Gojobori WH Li D Graur, J Mol Evol 1982 18 360 369 7120431
45. Pseudogenes as a paradigm of neutral evolution. WH Li T Gojobori M Nei, Nature 1981 292 237 239 7254315
46. Pseudogenes: are they "junk" or functional DNA? ES Balakirev FJ Ayala, Annu Rev Genet 2003 37 123 151 14616058
47. Nucleotide variation of the Est-6 gene region in natural populations of Drosophila melanogaster. ES Balakirev FJ Ayala, Genetics 2003 165 1901 1914 14704175
48. Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. N Echols P Harrison S Balasubramanian NM Luscombe P Bertone Z Zhang M Gerstein, Nucleic Acids Res 2002 30 2515 2523 12034841
49. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. E Zouros AO Ball C Saavedra KR Freeman, Proc Natl Acad Sci USA 1994 91 7463 7467 8052604
50. The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: Implications for the operation of doubly uniparental inheritance of mitochondrial DNA. MA Garrido-Ramos DT Stewart BW Sutherland E Zouros, Genome 1998 41 818 824
51. Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae). AC Dalziel DT Stewart, Genome 2002 45 348 355 11962632
52. Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. C Saavedra M-I Reyero E Zouros, Genetics 1997 145 1073 1082 9093859
53. The exceptional mitochondrial DNA system of the mussel family Mytilidae. E Zouros, Genes Genet Syst 2000 75 313 318 11280005
54. Genetics of mother-dependent sex ratio in Blue Mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. E Kenchington B MacDonald L Cao D Tsagkarakis E Zouros, Genetics 2002 161 1579 1588 12196402
55. Maternal inheritance, sexual conflict and the maladapted male. JA Zeh DW Zeh, Trends Genet 2005 21 281 286 15851064
56. A Burt R Trivers, Genes in Conflict: The Biology of Selfish Genetic Elements Cambridge: Belknap Press, Cambridge 2006
57. Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. EC Metz R Robles-Sikisaka VD Vacquier, Proc Natl Acad Sci USA 1998 95 10676 10681 9724763
58. The rapid evolution of reproductive proteins. WJ Swanson VD Vacquier, Nat Rev Genet 2002 3 137 144 11836507
59. Evolution of reproductive proteins from animals and plants. NL Clark JE Aagaard WJ Swanson, Reproduction 2006 131 11 22 16388004
60. Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). L Cao ELR Kenchington E Zouros, Genetics 2004 166 883 894 15020473
61. Segregation of sperm mitochondria in two- and four cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. AT Cogswell ELR Kenchington E Zouros, Genome 2006 49 799 807 16936788
62. Primers for amplifying the hypervariable, male-transmitted COII-COI junction region in amblemine freshwater mussels (Bivalvia: Unionoidea: Ambleminae). JM Walker AE Bogan EA Bonfiglio DC Campbell AD Christian JP Curole JL Harris RJ Wojtecki WR Hoeh, Mol Ecol Notes 2007 7 489 491
63. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. O Folmer M Black WR Hoeh R Lutz R Vrijenhoek, Mol Mar Biol Biotechnol 1994 3 294 299 7881515
64. WP Maddison DR Maddison, MacClade: Analysis of Phylogeny and Character Evolution Sunderland: Sinauer Assoc., Inc 2000
65. The Pfam protein families database. A Bateman L Coin R Durbin RD Finn V Hollich S Griffiths-Jones A Khanna M Marshall S Moxon ELL Sonnhammer DJ Studholme C Yeats SR Eddy, Nucleic Acids Res 2004 32 138 141
66. ConPred II: a consensus prediction method for obtaining transmembrane topology models with high reliability. M Arai H Mitsuke M Ikeda JX Xia T Kikuchi M Satake T Shimizu, Nucleic Acids Res 2004 32 Web Server W390 393 15215417
67. MrBayes: Bayesian inference of phylogeny. JP Huelsenbeck F Ronquist, Bioinformatics 2003 17 754 755
68. MrBayes 3: Bayesian phylogenetic inference under mixed models. F Ronquist JP Huelsenbeck, Bioinformatics 2003 19 1572 1574 12912839
69. The general stochastic model of nucleotide substitution. F Rodriguez JL Oliver A Marin JR Medina, J Theor Biol 1990 142 485 501 2338834
70. Modeltest: Testing the model of DNA substitution. D Posada KA Crandall, Bioinformatics 1998 14 817 818 9918953
71. Accurate branch length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch length priors. DC Marshall C Simon TR Buckley, Syst Biol 2006 55 992 1003
72. DL Swofford, PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Sunderland: Sinauer Associates 2001
73. A likelihood approach to estimating phylogeny from discrete morphological character data. PO Lewis, Syst Biol 2001 50 913 925 12116640
74. WP Maddison DR Maddison, Mesquite: a modular system for evolutionary analysis. Version 1.05 2003 http://mesquiteproject.org
75. AWF Edwards, Likelihood Cambridge: Cambridge University Press 1972
76. The maximum likelihood approach to reconstructing ancestral character states on phylogenies. M Pagel, Syst Biol 1999 48 612 622
77. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order of the Hominoidea. H Kishino M Hasegawa, J Mol Evol 1989 29 170 179 2509717
78. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the humans and apes. AR Templeton, Evolution 1983 37 221 244
79. Ancient origin of lactabumin from lysozyme: analysis of DNA and amino acid sequences. EM Prager AC Wilson, J Mol Evol 1988 27 326 335 3146643
80. An approximately unbiased test of phylogenetic tree selection. H Shimodaira, Syst Biol 2002 51 492 508 12079646
81. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. H Shimodaira M Hasegawa, Mol Biol Evol 1999 16 1114 1116
82. CONSEL: for assessing the confidence of phylogenetic tree selection. H Shimodaira H Hasegawa, Bioinformatics 2001 17 1246 1247 11751242
83. PAML: A program package for phylogenetic analysis by maximum likelihood. ZH Yang, Comput Appl Biosci 1997 13 555 556 9367129
84. Models of amino acid substitution and applications to mitochondrial protein evolution. ZH Yang R Nielsen M Hasegawa, Mol Biol Evol 1998 15 1600 1611 9866196
85. The PROSITE database, its status in 1997. A Bairoch P Bucher K Hofmann, Nucleic Acids Res 1997 25 217 221 9016539
86. HyPhy: hypothesis testing using phylogenies. SL Kosakovsky Pond SDW Frost SV Muse, Bioinformatics 2005 21 676 679 15509596
87. Bayes empirical Bayes inference of amino acid sites under positive selection. ZH Yang WSW Wong R Nielsen, Mol Biol Evol 2005 22 1107 1118 15689528
88. Adaptive evolution of scorpion sodium channel toxins. S Zhu F Bosmans J Tytgat, J Mol Evol 2004 58 145 153 15042334
89. Not so different after all: A comparison of methods for detecting amino acid sites under selection. SL Kosakovsky Pond SDW Frost, Mol Biol Evol 2005 22 1208 1222 15703242
90. Codon-based detection of positive selection can be biased by heterogenous distribution of polar amino acids along protein sequences. X Xia S Kumar, Comput Syst Bioinformatics conf 2006 4 335 340
91. Accuracy and power of bayes prediction of amino acid sites under positive selection. M Anisimova JP Bielawski Z Yang, Mol Biol Evol 2002 19 950 958 12032251
92. Site-to-site variation of synonymous substitution rates. SL Kosakovsky Pond SV Muse, Mol Biol Evol 2005 22 2375 2385 16107593
93. TreeSAAP: Selection on amino acid properties using phylogenetic trees. S Woolley J Johnson MJ Smith KA Crandall DA McClellan, Bioinformatics 2003 19 671 672 12651734
94. Genetic codes as evolutionary filters: subtle differences in the structure of genetic codes result in significant differences in patterns of nucleotide substitution. DA McClellan DG Whiting RG Christensen JK Sailsbery, J Theoret Biol 2004 226 393 400
95. Nucleotide composition bias affects amino acid content in proteins coded by animal mitochondria. PG Foster LS Jermiin DA Hickey, J Mol Evol 1997 44 282 288 9060394