Complete sequences of organelle genomes from the medicinal plant Rhazya stricta (Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Park, Seongjun ^a   Ruhlman, Tracey A ^a   Sabir, Jamal S M ^b   Mutwakil, Mohammed H Z ^b   Baeshen, Mohammed N ^b   Sabir, Meshaal J ^b   Baeshen, Nabih A ^b   Jansen, Robert K ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Adfir; Asterids; Gene transfers; Harmal; Medicinal plant; Organelle genomes

Indexed keywords

ANGIOSPERM; APOCYNACEAE; ARTICLE; CLADISTICS; CONTROLLED STUDY; DNA TRANSFER; GENE DOSAGE; GENE LOSS; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; INTRON; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; PHYLOGENETIC TREE; PLANT GENOME; RHAZYA STRICTA; RPS14 GENE; SDH3 GENE; SEQUENCE ANALYSIS; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; MEDICINAL PLANT; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PLASTID; PLASTID GENOME; SEQUENCE ALIGNMENT; TRANSPOSON;

APOCYNACEAE; ASTERIDS; MAGNOLIOPHYTA; RHAZYA; RHAZYA STRICTA;

TRANSPOSON; VEGETABLE PROTEIN;

APOCYNACEAE; BASE SEQUENCE; BIOLOGICAL EVOLUTION; DNA TRANSPOSABLE ELEMENTS; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; GENOME, PLANT; GENOME, PLASTID; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; PLANT PROTEINS; PLANTS, MEDICINAL; PLASTIDS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 84901667125     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-405     Document Type: Article

References (82)

1. Ageel AM, Mossa JS, Al-Yahya MA, Tariq M, Al-Said MS. Plants Used in Saudi Folk Medicine 1987, Riyadh, Saudia Arabia: King Saud University Press.
2. Ali BH, Bashir AK, Banna NR, Tanira MO. Central nervous system activity of Rhazya stricta Dence in mice. Clin Exp Pharmacol Physiol 1995, 22:248-253. 10.1111/j.1440-1681.1995.tb01989.x, 7671436.
3. Ali BH, Bashir AK, Tanira MO. The effect of Rhazya stricta, a traditional medicinal plant, on the forced swimming test in rats. Pharmacol Biochem Behav 1998, 59:547-550. 10.1016/S0091-3057(97)00470-X, 9477006.
4. Ali BH, Al-Qarawi AA, Bashir AK, Tanira MO. Phytochemistry, pharmacology and toxicity of Rhazya stricta Decne: A review. Phytother Res 2000, 14:229-234. 10.1002/1099-1573(200006)14:4<229::AID-PTR673>3.0.CO;2-5, 10861963.
5. Gilani SA, Kikuchi A, Shinwari ZK, Khattak ZI, Watanabe KN. Phytochemical, pharmacological and ethnobotanical studies of Rhazya stricta Decne. Phytother Res 2007, 21:301-307. 10.1002/ptr.2064, 17186492.
6. Baeshen NA, Elkady AI, Abuzinadah OA, Mutwakil MH. Potential anticancer activity of the medicinal herb, Rhazya stricta, against human breast cancer. Afr J Biotechnol 2012, 11:8960-8972.
7. Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM, Larson TR, Li Y, Pawson T, Penfield T, Rae AM, Rathbone DA, Reid S, Ross J, Smallwood MF, Segura V, Townsend T, Vyas D, Winzer T, Bowles D. The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 2010, 327:328-331. 10.1126/science.1182612, 20075252.
8. Li Y, Luo HM, Sun C, Song JY, Sun YZ, Wu Q, Wang N, Yao H, Steinmetz A, Chen SL. EST analysis reveals putative genes involved in glycyrrhizin biosynthesis. BMC Genomics 2010, 11:268. 10.1186/1471-2164-11-268, 2886062, 20423525.
9. Fuller CW, Middendorf LR, Benner SA, Church GM, Harris T, Huang X, Jovanovich SB, Nelson JR, Schloss JA, Schwartz DC, Vezenov DV. The challenges of sequencing by synthesis. Nat Biotechnol 2009, 27:1013-1023. 10.1038/nbt.1585, 19898456.
10. Voelkerding KV, Dames SA, Durtschi JD. Next-generation sequencing: from basic research to diagnostics. Clin Chem 2009, 55:641-658. 10.1373/clinchem.2008.112789, 19246620.
11. Metzker ML. Sequencing technologies - the next generation. Nat Rev Genet 2010, 11:31-46. 10.1038/nrg2626, 19997069.
12. Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 2012, 13:36-46.
13. Bock R. Structure, function, and inheritance of plastid genomes. 2007, 19:29-63. Berlin Heidelberg: Springer, Bock R, Cell and Molecular Biology of Plastids.
14. Jansen RK, Ruhlman TA. Plastid genomes of seed plants. Genomics of Chloroplasts and Mitochondria 2012, 103-126. New York: Springer, Bock R, Knoop V.
15. Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N. The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol 2007, 24:699-709.
16. 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.
17. Mower JP, Sloan DB, Alverson AJ. Plant mitochondrial genome diversity: the genomics revolution. Plant genome diversity volume 1: plant genomes, their residents, and their evolutionary dynamics 2012, 123-144. New York: Springer, Wendel JH.
18. Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nasuda S, Nakamura C, Mori N, Takumi S, Murata M, Futo S, Tsunewaki K. Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res 2005, 33:6235-6250. 10.1093/nar/gki925, 1275586, 16260473.
19. 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.
20. Sloan DB, Alverson AJ, Storchová 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.
21. 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.
22. Mower JP, Case AL, Floro ER, Willis JH. Evidence against equimolarity of large repeat arrangements and a predominant master circle structure of the mitochondrial genome from a monkeyflower (Mimulus guttatus) lineage with cryptic CMS. Genome Biol Evol 2012, 4:670-686. 10.1093/gbe/evs042, 3381676, 22534162.
23. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA. Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 2007, 19:1251-1264. 10.1105/tpc.106.048355, 1913765, 17468263.
24. Hanson MR, Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 2004, 16:S154-S169. 10.1105/tpc.015966, 2643387, 15131248.
25. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135. 10.1038/nrg1271, 14735123.
26. Goremykin VV, Salamini F, Velasco R, Viola R. Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 2009, 26:99-110.
27. 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.
28. Rodríguez-Moreno L, González VM, Benjak A, Martí MC, Puigdomènech P, Aranda MA, Garcia-Mas J. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics 2011, 12:424. 10.1186/1471-2164-12-424, 3175227, 21854637.
29. Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, de Pamphilis CW, Knox EB, Palmer JD. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 2013, 342:1468-1473. 10.1126/science.1246275, 24357311.
30. Covello PS, Gray MW. RNA editing in plant mitochondria. Nature 1989, 341:662-666. 10.1038/341662a0, 2552326.
31. Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V. Plant mitochondrial RNA editing. J Mol Evol 1999, 48:303-312. 10.1007/PL00006473, 10093219.
32. Glaser E, Soll J. Targeting signals and import machinery of plastids and plant mitochondria. Molecular Biology and Biotechnology of Plant Organelles: Chloroplasts and Mitochondria 2004, 385-418. New York: Springer, Daniell H, Chase C.
33. Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 2003, 29:380-395. 10.1016/S1055-7903(03)00194-5, 14615181.
34. Ueda M, Fujimoto M, Arimura S, Murata J, Tsutsumi N, Kadowaki K. Loss of the rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene 2007, 402:51-56. 10.1016/j.gene.2007.07.019, 17728076.
35. Jansen RK, Saski C, Lee SB, Hansen AK, Daniell H. Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 2011, 28:835-847. 10.1093/molbev/msq261, 3108605, 20935065.
36. Liu SL, Zhuang Y, Zhang P, Adams KL. Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus. Mol Biol Evol 2009, 26:875-891. 10.1093/molbev/msp011, 19168566.
37. Raubeson LA, Jansen RK. Chloroplast genomes of plants. Plant diversity and evolution: genotypic and phenotypic variation in higher plants 2005, 45-68. Cambridge MA: CABI, Henry RJ.
38. Weng ML, Blazier JC, Govindu M, Jansen RK. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Mol Biol Evol 2013, 31:645-659.
39. Straub SC, Cronn RC, Edwards C, Fishbein M, Liston A. Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biol Evol 2013, 5:1872-1885. 10.1093/gbe/evt140, 3814198, 24029811.
40. Iorizzo M, Senalik D, Szklarczyk M, Grzebelus D, Spooner D, Simon P. De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biol 2012, 12:61. 10.1186/1471-2229-12-61, 3413510, 22548759.
41. Conklin PL, Hanson MR. Recombination of plant mitochondrial genomes. Homologous Recombination and Gene Silencing in Plants 1994, 61-81. Netherlands: Springer, Paszkowski J.
42. Marienfeld J, Unseld M, Brandt P, Brennicke A. Genomic recombination of the mitochondrial atp6 gene in Arabidopsis thaliana at the protein processing site creates two different presequences. DNA Res 1996, 3:287-290. 10.1093/dnares/3.5.287, 9039497.
43. 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.
44. Maréchal-Drouard L, Guillemaut P, Cosset A, Arbogast M, Weber F, Weil JH, Dietrich A. Transfer RNAs of potato (Solanum tubeosum) mitochondria have different genetic origins. Nucleic Acids Res 1990, 18:3689-3696. 10.1093/nar/18.13.3689, 331066, 2374706.
45. Wang D, Wu YW, Shih AC, Wu CS, Wang YN, Chaw SM. 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.
46. Richardson AO, Rice DW, Young GJ, Alverson AJ, Palmer JD. The " fossilized" mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biol 2013, 11:29. 10.1186/1741-7007-11-29, 3646698, 23587068.
47. 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.
48. Holec S, Lange H, Kühn K, Alioua M, Börner T, Gagliardi D. Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol Cell Biol 2006, 26:2869-2876. 10.1128/MCB.26.7.2869-2876.2006, 1430307, 16537927.
49. 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.
50. Cusimano N, Zhang LB, Renner SS. Reevaluation of the cox1 group I intron in Araceae and angiosperms indicates a history dominated by loss rather than horizontal transfer. Mol Biol Evol 2008, 25:265-276. 10.1093/molbev/msm241, 18158323.
51. Mower JP, Jain K, Hepburn NJ. The role of horizontal transfer in shaping the plant mitochondrial genome. Advances in Botanical Research Volume 63: Mitochondrial Genome Evolution 2012, 41-69. New York: Academic Press, Maréchal-Drouard L.
52. 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 U S A 2002, 99:9905-9912. 10.1073/pnas.042694899, 126597, 12119382.
53. Adams KL, Rosenblueth M, Qiu YL, Palmer JD. Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. Genetics 2001, 158:1289-1300. 1461739, 11454775.
54. Ong HC, Palmer JD. Pervasive survival of expressed mitochondrial rps14 pseudogenes in grasses and their relatives for 80 million years following three functional transfers to the nucleus. BMC Evol Biol 2006, 6:55. 10.1186/1471-2148-6-55, 1543663, 16842621.
55. Adams KL, Song K, Roessler PG, Nugent JM, Doyle JL, Doyle JJ, Palmer JD. Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc Natl Acad Sci U S A 1999, 96:13863-13868. 10.1073/pnas.96.24.13863, 24156, 10570164.
56. Sandoval P, León G, Gómez I, Carmona R, Figueroa P, Holuigue L, Araya A, Jordana X. Transfer of RPS14 and RPL5 from the mitochondrion to the nucleus in grasses. Gene 2004, 324:139-147.
57. Choi C, Liu Z, Adams KL. Evolutionary transfers of mitochondrial genes to the nucleus in the Populus lineage and coexpression of nuclear and mitochondrial Sdh4 genes. New Phytol 2006, 172:429-439. 10.1111/j.1469-8137.2006.01821.x, 17083674.
58. Maréchal A, Brisson N. Recombination and the maintenance of plant organelle genome stability. New Phytol 2010, 186:299-317. 10.1111/j.1469-8137.2010.03195.x, 20180912.
59. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987, 19:11-15.
60. Koren S, Schatz MC, Walenz BP, Martin J, Howard JT, Ganapathy G, Wang Z, Rasko DA, McCombie WR, Jarvis ED, Phillippy AM. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat Biotechnol 2012, 30:693-700. 10.1038/nbt.2280, 3707490, 22750884.
61. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829. 10.1101/gr.074492.107, 2336801, 18349386.
62. Biomatters Geneious R6 v.6.1.6. [http://www.geneious.com/], Biomatters.
63. Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 2004, 20:3252-3255. 10.1093/bioinformatics/bth352, 15180927.
64. Dombrovska O, Qiu YL. Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 2004, 32:246-263. 10.1016/j.ympev.2003.12.013, 15186811.
65. Lowe TM, Eddy SR. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964. 10.1093/nar/25.5.0955, 146525, 9023104.
66. Lohse M, Drechsel O, Kahlau S, Bock R. OrganellarGenomeDRAW - a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 2013, 41:W575-W581. 10.1093/nar/gkt289, 3692101, 23609545.
67. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.
68. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3 - new capabilities and interfaces. Nucleic Acids Res 2012, 40:e115. 10.1093/nar/gks596, 3424584, 22730293.
69. The NCBI ORF finder. [http://www.ncbi.nlm.nih.gov/gorf/gorf.html].
70. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580. 10.1006/jmbi.2000.4315, 11152613.
71. Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 2006, 7:474. 10.1186/1471-2105-7-474, 1634758, 17064419.
72. Mower JP. The PREP Suite: Predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res 2009, 37:W253-W259. 10.1093/nar/gkp337, 2703948, 19433507.
73. Lenz H, Knoop V. PREPACT 2.0: Predicting C-to-U and U-to-C RNA editing in organelle genome sequences with multiple references and curated RNA editing annotation. Bioinfrom Biol Insights 2013, 7:1-19.
74. Zhang J, Ruhlman TA, Mower JP, Jansen RK. Comparative analyses of two Geraniaceae transcriptomes using next-generation sequencing. BMC Plant Biol 2013, 13:228. 10.1186/1471-2229-13-228, 3880972, 24373163.
75. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652. 10.1038/nbt.1883, 3571712, 21572440.
76. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2007, 2:953-971. 10.1038/nprot.2007.131, 17446895.
77. Small I, Peeters N, Legeai F, Lurin C. Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 2004, 4:1581-1590. 10.1002/pmic.200300776, 15174128.
78. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 2012, 40:D1178-D1186. 10.1093/nar/gkr944, 3245001, 22110026.
79. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 2013, 41:D348-D352. 10.1093/nar/gks1243, 3531192, 23197659.
80. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
81. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446, 16928733.
82. Geer LY, Domrachev M, Lipman DJ, Bryant SH. CDART: protein homology by domain architecture. Genome Res 2002, 12:1619-1623. 10.1101/gr.278202, 187533, 12368255.