The "fossilized" mitochondrial genome of Liriodendron tulipifera: Ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate

BMC Biology

Volumn 11, Issue , 2013, Pages

  Richardson, Aaron O ^a   Rice, Danny W ^a   Young, Gregory J ^a,b   Alverson, Andrew J ^c   Palmer, Jeffrey D ^a  

^a INDIANA UNIVERSITY   (United States)

^b DUPONT COMPANY   (United States)

^c UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Angiosperm; Intracellular gene transfer; Mitochondrial genome; Molecular evolution; RNA editing; Substitution rate

Indexed keywords

CALYCANTHUS FLORIDUS; LILIOPSIDA; LIRIODENDRON; LIRIODENDRON TULIPIFERA; MAGNOLIA; MAGNOLIA STELLATA; MAGNOLIACEAE; MAGNOLIIDAE; MAGNOLIIDS; MAGNOLIOPHYTA;

CHLOROPLAST DNA; TRANSFER RNA;

ARTICLE; BASE PAIRING; FOSSIL; GENE ORDER; GENETICS; GENOME SIZE; LIRIODENDRON; MITOCHONDRIAL GENOME; MOLECULAR EVOLUTION; MULTIGENE FAMILY; MUTATION RATE; PLASTID; RNA EDITING;

BASE PAIRING; DNA, CHLOROPLAST; EVOLUTION, MOLECULAR; FOSSILS; GENE ORDER; GENOME SIZE; GENOME, MITOCHONDRIAL; LIRIODENDRON; MULTIGENE FAMILY; MUTATION RATE; PLASTIDS; RNA EDITING; RNA, TRANSFER;

EID: 84876144707     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-29     Document Type: Article

References (90)

1. Handa H. The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 2003, 31:5907-5916. 10.1093/nar/gkg795, 219474, 14530439.
2. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 2012, 10:e1001241. 10.1371/journal.pbio.1001241, 3260318, 22272183.
3. Mower JP, Sloan DB, Alverson AJ. Plant mitochondrial genome diversity: the genomics revolution. Plant Genome Diversity 2012, 1:123-144. Vienna: Springer Vienna, Wendel JF, Greilhuber J, Dolezel J, Leitch IJ.
4. Chapdelaine Y, Bonen L. The wheat mitochondrial gene for subunit 1 of the NADH dehydrogenase complex: a trans-splicing model for the gene-in-pieces. Cell 1991, 65:465-472. 10.1016/0092-8674(91)90464-A, 1902143.
5. Adams KL, Qiu YL, Stoutemyer M, Palmer JD. Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci USA 2002, 99:9905-9912. 10.1073/pnas.042694899, 126597, 12119382.
6. Unseld M, Marienfeld JR, Brandt P, Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 1997, 15:57-61.
7. Joyce PB, Gray MW. Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res 1989, 17:5461-5476. 10.1093/nar/17.14.5461, 318170, 2762145.
8. Kitazaki K, Kubo T, Kagami H, Matsumoto T, Fujita A, Matsuhira H, Matsunaga M, Mikami T. A horizontally transferred tRNACys gene in the sugar beet mitochondrial genome: evidence that the gene is present in diverse angiosperms and its transcript is aminoacylated. Plant J 2011, 68:262-272. 10.1111/j.1365-313X.2011.04684.x, 21699590.
9. Wolfe KH, Li WH, Sharp PM. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 1987, 84:9054-9058. 10.1073/pnas.84.24.9054, 299690, 3480529.
10. Mower JP, Touzet P, Gummow JS, Delph LF, Palmer JD. Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol Biol 2007, 7:135. 10.1186/1471-2148-7-135, 1973135, 17688696.
11. Cho Y, Mower JP, Qiu YL, Palmer JD. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc Natl Acad Sci USA 2004, 101:17741-17746. 10.1073/pnas.0408302101, 539783, 15598738.
12. Sloan DB, Barr CM, Olson MS, Keller SR, Taylor DR. Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA. Mol Biol Evol 2008, 25:243-246. 10.1093/molbev/msm266, 18056075.
13. Palmer JD, Herbon LA. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 1988, 28:87-97. 10.1007/BF02143500, 3148746.
14. Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD. Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 2010, 27:1436-1448. 10.1093/molbev/msq029, 2877997, 20118192.
15. Satoh M, Kubo T, Nishizawa S, Estiati A, Itchoda N, Mikami T. The cytoplasmic male-sterile type and normal type mitochondrial genomes of sugar beet share the same complement of genes of known function but differ in the content of expressed ORFs. Mol Genet Genomics 2004, 272:247-256. 10.1007/s00438-004-1058-9, 15340837.
16. Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 2005, 272:603-615. 10.1007/s00438-004-1075-8, 15583938.
17. Perrotta G, Regina T, Quagliariello C, Ceci L. Conservation of the organization of the mitochondrial nad3 and rps12 genes in evolutionarily distant angiosperms. Mol Gen Genet 1996, 251:326-337.
18. Quiñones V, Zanlungo S, Moenne A, Gómez I, Holuigue L, Litvak S, Jordana X. The rpl5-rps14-cob gene arrangement in Solanum tuberosum: rps14 is a transcribed and unedited pseudogene. Plant Mol Biol 1996, 31:937-943. 10.1007/BF00019483, 8806426.
19. Takemura M, Oda K, Yamato K, Ohta E, Nakamura Y, Nozato N, Akashi K, Ohyama K. Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. Nucleic Acids Res 1992, 20:3199-3205. 10.1093/nar/20.12.3199, 312459, 1620617.
20. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA - a primitive form of plant mitochondrial genome. J Mol Biol 1992, 223:1-7. 10.1016/0022-2836(92)90708-R, 1731062.
21. Giegé P, Brennicke A. RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 1999, 96:15324-15329. 10.1073/pnas.96.26.15324, 24818, 10611383.
22. Covello PS, Gray MW. RNA editing in plant mitochondria. Nature 1989, 341:662-666. 10.1038/341662a0, 2552326.
23. Hiesel R, Wissinger B, Schuster W, Brennicke A. RNA editing in plant mitochondria. Science 1989, 246:1632-1634. 10.1126/science.2480644, 2480644.
24. Gualberto JM, Lamattina L, Bonnard G, Weil J-H, Grienenberger J-M. RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 1989, 341:660-662. 10.1038/341660a0, 2552325.
25. Sloan DB, MacQueen AH, Alverson AJ, Palmer JD, Taylor DR. Extensive loss of RNA editing sites in rapidly evolving Silene mitochondrial genomes: selection vs. retroprocessing as the driving force. Genetics 2010, 185:1369-1380. 10.1534/genetics.110.118000, 2927763, 20479143.
26. Mower JP. Modeling sites of RNA editing as a fifth nucleotide state reveals progressive loss of edited sites from angiosperm mitochondria. Mol Biol Evol 2008, 25:52-61.
27. Shields DC, Wolfe KH. Accelerated evolution of sites undergoing mRNA editing in plant mitochondria and chloroplasts. Mol Biol Evol 1997, 14:344-349. 10.1093/oxfordjournals.molbev.a025768, 9066800.
28. Chaw SM, Shih AC, Wang D, Wu YW, Liu SM, Chou TY. The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Mol Biol Evol 2008, 25:603-615. 10.1093/molbev/msn009, 18192697.
29. Salmans M, Chaw S-M, Lin C-P, Shih A, Wu Y-W, Mulligan R. Editing site analysis in a gymnosperm mitochondrial genome reveals similarities with angiosperm mitochondrial genomes. Curr Genet 2010, 56:439-446. 10.1007/s00294-010-0312-4, 2943580, 20617318.
30. Magallón S. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Syst Biol 2010, 59:384-399. 10.1093/sysbio/syq027, 20538759.
31. Smith SA, Beaulieu JM, Donoghue MJ. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci USA 2010, 107:5897-5902. 10.1073/pnas.1001225107, 2851901, 20304790.
32. Grewe F, Viehoever P, Weisshaar B, Knoop V. A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 2009, 37:5093-5104. 10.1093/nar/gkp532, 2731911, 19553190.
33. Angiosperm Phylogeny Group An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 2009, 161:105-121. Angiosperm Phylogeny Group.
34. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Latvis M, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, Gitzendanner MA, Sytsma KJ, Qiu Y-L, Hilu KW, Davis CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS. Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot 2011, 98:704-730. 10.3732/ajb.1000404, 21613169.
35. Bendich AJ. Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. J Mol Biol 1996, 255:564-588. 10.1006/jmbi.1996.0048, 8568898.
36. Sloan DB, Müller K, McCauley DE, Taylor DR, Štorchová H. Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol 2012, 196:1228-1239. 10.1111/j.1469-8137.2012.04340.x, 23009072.
37. Lohse M, Drechsel O, Bock R. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 2007, 52:267-274. 10.1007/s00294-007-0161-y, 17957369.
38. Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 2011, 23:2499-2513. 10.1105/tpc.111.087189, 3226218, 21742987.
39. Sloan DB, Alverson AJ, Storchova H, Palmer JD, Taylor DR. Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol 2010, 10:274. 10.1186/1471-2148-10-274, 2942850, 20831793.
40. Alverson AJ, Zhuo S, Rice DW, Sloan DB, Palmer JD. The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS One 2011, 6:e16404. 10.1371/journal.pone.0016404, 3024419, 21283772.
41. Sanchez-Puerta MV, Cho Y, Mower JP, Alverson AJ, Palmer JD. Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria. Mol Biol Evol 2008, 25:1762-1777. 10.1093/molbev/msn129, 2727383, 18524785.
42. Cho Y, Qiu YL, Kuhlman P, Palmer JD. Explosive invasion of plant mitochondria by a group I intron. Proc Natl Acad Sci USA 1998, 95:14244-14249. 10.1073/pnas.95.24.14244, 24358, 9826685.
43. Qiu YL, Palmer JD. Many independent origins of trans splicing of a plant mitochondrial group II intron. J Mol Evol 2004, 59:80-89.
44. Regina T, Picardi E, Lopez L, Pesole G, Quagliariello C. A novel additional group II intron distinguishes the mitochondrial rps3 gene in gymnosperms. J Mol Evol 2005, 60:196-206. 10.1007/s00239-004-0098-4, 15785848.
45. Regina TM, Quagliariello C. Lineage-specific group II intron gains and losses of the mitochondrial rps3 gene in gymnosperms. Plant Physiol Biochem 2010, 48:646-654. 10.1016/j.plaphy.2010.05.003, 20605476.
46. Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T. The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucleic Acids Res 2000, 28:2571-2576. 10.1093/nar/28.13.2571, 102699, 10871408.
47. Forner J, Weber B, Thuss S, Wildum S, Binder S. Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res 2007, 35:3676-3692. 10.1093/nar/gkm270, 1920247, 17488843.
48. Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol 2012, 4:294-306. 10.1093/gbe/evs006, 3318436, 22247429.
49. Nie Z-L, Wen J, Azuma H, Qiu Y-L, Sun H, Meng Y, Sun W-B, Zimmer EA. Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear data sets. Mol Phylogen Evol 2008, 48:1027-1040.
50. Parks C, Wendel JF. Molecular divergence between Asian and North American species of Liriodendron (Magnoliaceae) with implications for interpretation of fossil floras. Am J Bot 1990, 77:1243-1256.
51. Drouin G, Daoud H, Xia J. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogen Evol 2008, 49:827-831.
52. Eyre-Walker A, Gaut BS. Correlated rates of synonymous site evolution across plant genomes. Mol Biol Evol 1997, 14:455-460. 10.1093/oxfordjournals.molbev.a025781, 9100375.
53. Guisinger MM, Kuehl JV, Boore JL, Jansen RK. Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA 2008, 105:18424-18429. 10.1073/pnas.0806759105, 2587588, 19011103.
54. Wang D, Wu Y-W, Shih AC, Wu C-S, Wang Y-N, Chaw S-M. Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 mya. Mol Biol Evol 2007, 24:2040-2048. 10.1093/molbev/msm133, 17609537.
55. Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 2002, 268:434-445. 10.1007/s00438-002-0767-1, 12471441.
56. Kubo T, Mikami T. Organization and variation of angiosperm mitochondrial genome. Physiol Plant 2007, 129:6-13.
57. Clifton SW, Minx P, Fauron CM, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ. Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 2004, 136:3486-3503. 10.1104/pp.104.044602, 527149, 15542500.
58. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG. Sequence and organization of the human mitochondrial genome. Nature 1981, 290:457-465. 10.1038/290457a0, 7219534.
59. Green RE, Malaspinas A-S, Krause J, Briggs AW, Johnson PL, Uhler C, Meyer M, Good JM, Maricic T, Stenzel U, Prüfer K, Siebauer M, Burbano HA, Ronan M, Rothberg JM, Egholm M, Rudan P, Brajković D, Kućan Z, Gusić I, Wikström M, Laakkonen L, Kelso J, Slatkin M, Pääbo S. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell 2008, 134:416-426. 10.1016/j.cell.2008.06.021, 2602844, 18692465.
60. Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Pääbo S. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 2010, 464:894-897. 10.1038/nature08976, 20336068.
61. Horai S, Hayasaka K, Kondo R, Tsugane K, Takahata N. Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc Natl Acad Sci USA 1995, 92:532-536. 10.1073/pnas.92.2.532, 42775, 7530363.
62. Bell CD, Soltis DE, Soltis PS. The age and diversification of the angiosperms re-revisited. Am J Bot 2010, 97:1296-1303. 10.3732/ajb.0900346, 21616882.
63. Wikström N, Savolainen V, Chase MW. Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond, Ser B: Biol Sci 2001, 268:2211-2220.
64. Frumin SI, Friis EM. Liriodendroid seeds from the late cretaceous of Kazakhstan and North Carolina, USA. Rev Palaeobot Palynol 1996, 94:39-55.
65. Friis EM, Crane PR, Pederson KR. Fossil History of magnoliid angiosperms. Evolution and Diversification of Land Plants 1997, 121-156. Tokyo: Springer, Iwatsuki K, Raven PH.
66. Smith SA, Donoghue MJ. Rates of molecular evolution are linked to life history in flowering plants. Science 2008, 322:86-89. 10.1126/science.1163197, 18832643.
67. Gaut B, Yang L, Takuno S, Eguiarte LE. The patterns and causes of variation in plant nucleotide substitution rates. Annu Rev Ecol Evol Syst 2011, 42:245-266.
68. Takenaka M, Verbitskiy D, Vandermerwe J, Zehrmann A, Brennicke A. The process of RNA editing in plant mitochondria. Mitochondrion 2008, 8:35-46. 10.1016/j.mito.2007.09.004, 18326075.
69. Lynch M, Koskella B, Schaack S. Mutation pressure and the evolution of organelle genomic architecture. Science 2006, 311:1727-1730. 10.1126/science.1118884, 16556832.
70. Gray MW, Covello PS. RNA editing in plant mitochondria and chloroplasts. FASEB J 1993, 7:64-71.
71. Gray MW, Lukeš J, Archibald JM, Keeling PJ, Doolittle WF. Irremediable complexity?. Science 2010, 330:920-921. 10.1126/science.1198594, 21071654.
72. Stoltzfus A. On the possibility of constructive neutral evolution. J Mol Evol 1999, 49:169-181. 10.1007/PL00006540, 10441669.
73. Mower JP. PREP-Mt: predictive RNA editor for plant mitochondrial genes. BMC Bioinforma 2005, 6:96.
74. Liu Y, Wang B, Cui P, Li L, Xue J-Y, Yu J, Qiu Y-L. The mitochondrial genome of the lycophyte Huperzia squarrosa: the most archaic form in vascular plants. PLoS One 2012, 7:e35168. 10.1371/journal.pone.0035168, 3325193, 22511984.
75. Jansen RK, Cai Z, Raubeson LA, Daniell H, de Pamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 2007, 104:19369-19374. 10.1073/pnas.0709121104, 2148296, 18048330.
76. Sandbrink JM, Vellekoop P, Vanham R, Vanbrederode J. A method for evolutionary studies on RFLP of chloroplast DNA, applicable to a range of plant species. Biochem Syst Ecol 1989, 17:45-49.
77. Sambrook J, Russell D. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 3.
78. Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res 1999, 9:868-877. 10.1101/gr.9.9.868, 310812, 10508846.
79. Goecks J, Nekrutenko A, Taylor J, Team TG. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. 10.1186/gb-2010-11-8-r86, 2945788, 20738864.
80. Bahloul M, Burkard G. An improved method for the isolation of total RNA from spruce tissues. Plant Mol Biol Rep 1993, 11:212-215.
81. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987, 19:11-15.
82. Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 2004, 101:17747-17752. 10.1073/pnas.0408336102, 539785, 15598737.
83. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
84. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
85. Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679. 10.1093/bioinformatics/bti079, 15509596.
86. Muse SV, Gaut BS. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol 1994, 11:715-724.
87. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. 10.1186/1471-2148-7-214, 2247476, 17996036.
88. Doyle JA, Hotton CL. Diversification of early angiosperm pollen in a cladistic context. Pollen and Spores: Patterns of Diversification 1991, 169-195. Oxford, UK: Clarendon Press, Blackmore S, Barnes SH.
89. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA. The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biol 2008, 14:2963-2977.
90. Csu{double acute}ös M. Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 2010, 26:1910-1912. 10.1093/bioinformatics/btq315, 20551134.