Genome of the Komodo dragon reveals adaptations in the cardiovascular and chemosensory systems of monitor lizards

. 2019 Aug ; 3 (8) : 1241-1252. [epub] 20190729

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31358948

Grantová podpora
UM1 HL098179 NHLBI NIH HHS - United States
U01 HL131003 NHLBI NIH HHS - United States
T32 HL007731 NHLBI NIH HHS - United States
T32 AR007175 NIAMS NIH HHS - United States
R01 HG005946 NHGRI NIH HHS - United States

Odkazy

PubMed 31358948
PubMed Central PMC6668926
DOI 10.1038/s41559-019-0945-8
PII: 10.1038/s41559-019-0945-8
Knihovny.cz E-zdroje

Monitor lizards are unique among ectothermic reptiles in that they have high aerobic capacity and distinctive cardiovascular physiology resembling that of endothermic mammals. Here, we sequence the genome of the Komodo dragon Varanus komodoensis, the largest extant monitor lizard, and generate a high-resolution de novo chromosome-assigned genome assembly for V. komodoensis using a hybrid approach of long-range sequencing and single-molecule optical mapping. Comparing the genome of V. komodoensis with those of related species, we find evidence of positive selection in pathways related to energy metabolism, cardiovascular homoeostasis, and haemostasis. We also show species-specific expansions of a chemoreceptor gene family related to pheromone and kairomone sensing in V. komodoensis and other lizard lineages. Together, these evolutionary signatures of adaptation reveal the genetic underpinnings of the unique Komodo dragon sensory and cardiovascular systems, and suggest that selective pressure altered haemostasis genes to help Komodo dragons evade the anticoagulant effects of their own saliva. The Komodo dragon genome is an important resource for understanding the biology of monitor lizards and reptiles worldwide.

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Chapman AD Numbers of Living Species in Australia and the World (Australian Biological Resources Study, 2009).

Collar DC, Schulte JA & Losos JB Evolution of extreme body size disparity in monitor lizards (Varanus). Evolution (N. Y). 65, 2664–2680 (2011). PubMed

Jensen B, Wang T, Christoffels VM & Moorman AFM Evolution and development of the building plan of the vertebrate heart. Biochim. Biophys. Acta - Mol. Cell Res 1833, 783–794 (2013). PubMed

Auffenberg W The Behavioral Ecology of the Komodo Monitor (University Presses of Florida, 1981).

Green B, King D, Braysher M & Saim A Thermoregulation, water turnover and energetics of free-living komodo dragons, Varanus komodoensis. Comp. Biochem. Physiol. Part A Physiol 99, 97–101 (1991).

Purwandana D et al. Ecological allometries and niche use dynamics across Komodo dragon ontogeny. Sci. Nat 103, 27 (2016). PubMed

Fry BG et al. A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus. Proc. Natl. Acad. Sci. U. S. A 106, 8969–8974 (2009). PubMed PMC

Koludarov I et al. Enter the Dragon: The Dynamic and Multifunctional Evolution of Anguimorpha Lizard Venoms. Toxins 9, (2017). PubMed PMC

Johnson Pokorná M et al. First Description of the Karyotype and Sex Chromosomes in the Komodo Dragon (Varanus komodoensis). Cytogenet. Genome Res 148, 284–291 (2016). PubMed

Iannucci A et al. Isolating Chromosomes of the Komodo Dragon: New Tools for Comparative Mapping and Sequence Assembly. Cytogenet. Genome Res 157, 42–50 (2019). PubMed

Gao J et al. Sequencing, de novo assembling, and annotating the genome of the endangered Chinese crocodile lizard Shinisaurus crocodilurus. Gigascience 6, 1–6 (2017). PubMed PMC

Alföldi J et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587–591 (2011). PubMed PMC

Simpson JT Exploring Genome Characteristics and Sequence Quality Without a Reference (2013). PubMed PMC

Krishan A et al. DNA index, genome size, and electronic nuclear volume of vertebrates from the Miami Metro Zoo. Cytom. Part A 65A, 26–34 (2005). PubMed

Doležel J, Bartoš J, Voglmayr H & Greilhuber J Letter to the editor. Cytom. Part A 51A, 127–128 (2003). PubMed

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV & Zdobnov EM BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015). PubMed

Rey R, Lukas-Croisier C, Lasala C & Bedecarrás P AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol 211, 21–31 (2003). PubMed

Rovatsos M, Rehák I, Velenský P & Kratochvíl L Shared ancient sex chromosomes in varanids, beaded lizards and alligator lizards. Mol. Biol. Evol (2019). doi:10.1093/molbev/msz024 PubMed DOI

Welton LJ, Travers SL, Siler CD & Brown RM Integrative taxonomy and phylogeny-based species delimitation of Philippine water monitor lizards (Varanus salvator Complex) with descriptions of two new cryptic species. Zootaxa 3881, 201 (2014). PubMed

Zheng Y & Wiens JJ Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol 94, 537–547 (2016). PubMed

Douglas ME, Douglas MR, Schuett GW, Beck DD & Sullivan BK Conservation phylogenetics of helodermatid lizards using multiple molecular markers and a supertree approach. Mol. Phylogenet. Evol 55, 153–167 (2010). PubMed

Castoe TA et al. Dynamic Nucleotide Mutation Gradients and Control Region Usage in Squamate Reptile Mitochondrial Genomes. Cytogenet. Genome Res 127, 112–127 (2009). PubMed PMC

Townsend TM et al. Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Mol. Phylogenet. Evol 61, 363–380 (2011). PubMed

Alfaro ME et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl. Acad. Sci 106, 13410–13414 (2009). PubMed PMC

Sanders KL & Lee MSY Molecular evidence for a rapid late-Miocene radiation of Australasian venomous snakes (Elapidae, Colubroidea). Mol. Phylogenet. Evol 46, 1165–1173 (2008). PubMed

Okajima Y & Kumazawa Y Mitogenomic perspectives into iguanid phylogeny and biogeography: Gondwanan vicariance for the origin of Madagascan oplurines. Gene 441, 28–35 (2009). PubMed

Kumazawa Y Mitochondrial genomes from major lizard families suggest their phylogenetic relationships and ancient radiations. Gene 388, 19–26 (2007). PubMed

Hugall AF, Foster R & Lee MSY Calibration Choice, Rate Smoothing, and the Pattern of Tetrapod Diversification According to the Long Nuclear Gene RAG-1. Syst. Biol 56, 543–563 (2007). PubMed

Wiens JJ, Brandley MC & Reeder TW Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles. Evolution 60, 123–41 (2006). PubMed

Pyron RA, Burbrink FT & Wiens JJ A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol 13, 93 (2013). PubMed PMC

Zheng Y & Wiens JJ Do missing data influence the accuracy of divergence-time estimation with BEAST? Mol. Phylogenet. Evol 85, 41–49 (2015). PubMed

Kumar S, Stecher G, Suleski M & Hedges SB TimeTree: A Resource for Timelines, Timetrees, and Divergence Times. Mol. Biol. Evol 34, 1812–1819 (2017). PubMed

Hsiang AY et al. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evol. Biol 15, 87 (2015). PubMed PMC

Tolley KA, Townsend TM & Vences M Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proc. R. Soc. B Biol. Sci 280, 20130184–20130184 (2013). PubMed PMC

Jones ME et al. Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara). BMC Evol. Biol 13, 208 (2013). PubMed PMC

Portik DM & Papenfuss TJ Monitors cross the Red Sea: The biogeographic history of Varanus yemenensis. Mol. Phylogenet. Evol 62, 561–565 (2012). PubMed

Pyron RA A Likelihood Method for Assessing Molecular Divergence Time Estimates and the Placement of Fossil Calibrations. Syst. Biol 59, 185–194 (2010). PubMed

Vidal N et al. Molecular evidence for an Asian origin of monitor lizards followed by Tertiary dispersals to Africa and Australasia. Biol. Lett 8, 853–855 (2012). PubMed PMC

Xiong Z et al. Draft genome of the leopard gecko, Eublepharis macularius. Gigascience 5, 47 (2016). PubMed PMC

Streicher JW & Wiens JJ Phylogenomic analyses of more than 4000 nuclear loci resolve the origin of snakes among lizard families. Biol. Lett 13, 20170393 (2017). PubMed PMC

Wiens JJ et al. Combining Phylogenomics and Fossils in Higher-Level Squamate Reptile Phylogeny: Molecular Data Change the Placement of Fossil Taxa. Syst. Biol 59, 674–688 (2010). PubMed

Fry BG et al. Early evolution of the venom system in lizards and snakes. Nature 439, 584–8 (2006). PubMed

Lee MSY Hidden support from unpromising data sets strongly unites snakes with anguimorph ‘lizards’. J. Evol. Biol 22, 1308–1316 (2009). PubMed

Silva L & Antunes A Vomeronasal Receptors in Vertebrates and the Evolution of Pheromone Detection. Annu. Rev. Anim. Biosci 5, 353–370 (2017). PubMed

Brykczynska U, Tzika AC, Rodriguez I & Milinkovitch MC Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles. Genome Biol. Evol 5, 389–401 (2013). PubMed PMC

Green RE et al. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science (80-.). 346, 1254449–1254449 (2014). PubMed PMC

Zippel HP The ecology of vertebrate olfaction. Behav. Processes 7, 198–199 (2002).

Yang H, Shi P, Zhang Y & Zhang J Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86, 306–315 (2005). PubMed

Fabregat A et al. The Reactome Pathway Knowledgebase. Nucleic Acids Res 46, D649–D655 (2018). PubMed PMC

Fabregat A et al. Reactome pathway analysis: a high-performance in-memory approach. BMC Bioinformatics 18, 142 (2017). PubMed PMC

Wu G & Haw R Functional Interaction Network Construction and Analysis for Disease Discovery. in Methods in molecular biology (Clifton, N.J.) 1558, 235–253 (2017). PubMed

Shultz AJ & Sackton T Immune genes are hotspots of shared positive selection across birds and mammals. Elife 8, (2019). PubMed PMC

Riquelme CA et al. Fatty Acids Identified in the Burmese Python Promote Beneficial Cardiac Growth. Science (80-.). 334, 528 LP – 531 (2011). PubMed PMC

Falkenberg M et al. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet 31, 289–294 (2002). PubMed

Cotney J, McKay SE & Shadel GS Elucidation of separate, but collaborative functions of the rRNA methyltransferase-related human mitochondrial transcription factors B1 and B2 in mitochondrial biogenesis reveals new insight into maternally inherited deafness. Hum. Mol. Genet 18, 2670–2682 (2009). PubMed PMC

Cho Y, Hazen BC, Russell AP & Kralli A Peroxisome Proliferator-activated Receptor γ Coactivator 1 (PGC-1)- and Estrogen-related Receptor (ERR)-induced Regulator in Muscle 1 (PERM1) Is a Tissue-specific Regulator of Oxidative Capacity in Skeletal Muscle Cells. J. Biol. Chem 288, 25207–25218 (2013). PubMed PMC

Cho Y et al. Perm1 enhances mitochondrial biogenesis, oxidative capacity, and fatigue resistance in adult skeletal muscle. FASEB J 30, 674–687 (2016). PubMed PMC

Zhao S et al. Regulation of Cellular Metabolism by Protein Lysine Acetylation. Science (80-.). 327, 1000–1004 (2010). PubMed PMC

Brzezniak LK, Bijata M, Szczesny RJ & Stepien PP Involvement of human ELAC2 gene product in 3’ end processing of mitochondrial tRNAs. RNA Biol 8, 616–626 (2011). PubMed

Holzmann J et al. RNase P without RNA: Identification and Functional Reconstitution of the Human Mitochondrial tRNA Processing Enzyme. Cell 135, 462–474 (2008). PubMed

Lee K-W & Bogenhagen DF Assignment of 2′-O-Methyltransferases to Modification Sites on the Mammalian Mitochondrial Large Subunit 16 S Ribosomal RNA (rRNA). J. Biol. Chem 289, 24936–24942 (2014). PubMed PMC

Cingolani HE et al. The Positive Inotropic Effect of Angiotensin II. Hypertension 47, 727–734 (2006). PubMed

Forrester SJ et al. Angiotensin II Signal Transduction: An Update on Mechanisms of Physiology and Pathophysiology. Physiol. Rev 98, 1627–1738 (2018). PubMed PMC

Kim S & Iwao H Molecular and Cellular Mechanisms of Angiotensin II-Mediated Cardiovascular and Renal Diseases. Pharmacol. Rev 52, 11 LP – 34 (2000). PubMed

Symons JD & Stebbins CL Effects of angiotensin II receptor blockade during exercise: comparison of losartan and saralasin. J. Cardiovasc. Pharmacol 28, 223–31 (1996). PubMed

Stebbins CL & Symons JD Role of angiotensin II in hemodynamic responses to dynamic exercise in miniswine. J. Appl. Physiol 78, 185–90 (1995). PubMed

WILSON JX The Renin-Angiotensin System in Nonmammalian Vertebrates. Endocr. Rev 5, 45–61 (1984). PubMed

Fournier D, Luft FC, Bader M, Ganten D & Andrade-Navarro MA Emergence and evolution of the renin–angiotensin–aldosterone system. J. Mol. Med 90, 495–508 (2012). PubMed PMC

Mueller CA, Eme J, Tate KB & Crossley DA Chronic captopril treatment reveals the role of ANG II in cardiovascular function of embryonic American alligators (Alligator mississippiensis). J. Comp. Physiol. B 188, 657–669 (2018). PubMed

Antl M et al. IRAG mediates NO/cGMP-dependent inhibition of platelet aggregation and thrombus formation. Blood 109, 552–559 (2007). PubMed

Puetz J & Boudreaux MK Evaluation of the gene encoding calcium and diacylglycerol regulated guanine nucleotide exchange factor I (CalDAG-GEFI) in human patients with congenital qualitative platelet disorders. Platelets 23, 401–403 (2012). PubMed

Bezman NA et al. Requirements of SLP76 tyrosines in ITAM and integrin receptor signaling and in platelet function in vivo. J. Exp. Med 205, 1775–88 (2008). PubMed PMC

Israels S & McMillan-Ward E CD63 modulates spreading and tyrosine phosphorylation of platelets on immobilized fibrinogen. Thromb. Haemost 93, 311–318 (2005). PubMed

Cooper DN, Millar DS, Wacey A, Pemberton S & Tuddenham EG Inherited factor X deficiency: molecular genetics and pathophysiology. Thromb. Haemost 78, 161–172 (1997). PubMed

Takahashi N, Takahashi Y & Putnam FW Primary structure of blood coagulation factor XIIIa (fibrinoligase, transglutaminase) from human placenta. Proc. Natl. Acad. Sci 83, 8019 LP – 8023 (1986). PubMed PMC

Mosesson MW The roles of fibrinogen and fibrin in hemostasis and thrombosis. Semin. Hematol 29, 177–188 (1992). PubMed

Pyron R, Burbrink FT & Wiens JJ A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol 13, 93 (2013). PubMed PMC

Pokorná M & Kratochvíl L Phylogeny of sex-determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc 156, 168–183 (2009).

Rovatsos M, Pokorna M, Altmanova M & Kratochvil L Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol. Lett 10, 20131093–20131093 (2014). PubMed PMC

Gamble T et al. Restriction Site-Associated DNA Sequencing (RAD-seq) Reveals an Extraordinary Number of Transitions among Gecko Sex-Determining Systems. Mol. Biol. Evol 32, 1296–1309 (2015). PubMed

Nielsen SV, Banks JL, Diaz RE, Trainor PA & Gamble T Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae). J. Evol. Biol 31, 484–490 (2018). PubMed

Rovatsos M, Altmanová M, Pokorná M & Kratochvíl L Conserved sex chromosomes across adaptively radiated anolis lizards. Evolution (N. Y). 68, 2079–2085 (2014). PubMed

Gamble T et al. The Discovery of XY Sex Chromosomes in a Boa and Python. Curr. Biol 27, 2148–2153.e4 (2017). PubMed

Emerson JJ Evolution: A Paradigm Shift in Snake Sex Chromosome Genetics. Curr. Biol 27, R800–R803 (2017). PubMed

Hattori RS et al. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc. Natl. Acad. Sci 109, 2955 LP – 2959 (2012). PubMed PMC

Cortez D et al. Origins and functional evolution of Y chromosomes across mammals. Nature 508, 488 (2014). PubMed

Bej DK, Miyoshi K, Hattori RS, Strüssmann CA & Yamamoto Y A Duplicated, Truncated amh Gene Is Involved in Male Sex Determination in an Old World Silverside. G3 Genes|Genomes|Genetics 7, 2489–2495 (2017). PubMed PMC

Ieda R et al. Identification of the sex-determining locus in grass puffer (Takifugu niphobles) provides evidence for sex-chromosome turnover in a subset of Takifugu species. PLoS One 13, e0190635 (2018). PubMed PMC

Halpern M Nasal chemical senses in reptiles: structure and function Pp 423–523 in Gans C, Crews D (eds) Biology of the Reptilia, Vol. 18, Brain. Horm. Behav Chicago/IL Univ. Chicago Press Google Sch; (1992).

Martin J & Lopez P Chemoreception, symmetry and mate choice in lizards. Proc. R. Soc. B Biol. Sci 267, 1265–1269 (2000). PubMed PMC

Baeckens S, Martín J, García-Roa R & van Damme R Sexual selection and the chemical signal design of lacertid lizards. Zool. J. Linn. Soc 183, 445–457 (2018).

van Damme R, Bauwens D, Thoen C, Vanderstighelen D & Verheyen RF Responses of Naive Lizards to Predator Chemical Cues. J. Herpetol 29, 38 (1995).

van Damme R & Castilla AM Chemosensory predator recognition in the lizard Podarcis hispanica: effects of predation pressure relaxation. J. Chem. Ecol 22, 13–22 (1996). PubMed

Cooper WE Correlated evolution of prey chemical discrimination with foraging, lingual morphology and vomeronasal chemoreceptor abundance in lizards. Behav. Ecol. Sociobiol 41, 257–265 (1997).

Cooper W Tandem evolution of diet and chemosensory responses in snakes. Amphibia-Reptilia 29, 393–398 (2008).

Hulbert AJ & Else PL Evolution of mammalian endothermic metabolism: mitochondrial activity and cell composition. Am. J. Physiol. Integr. Comp. Physiol 256, R63–R69 (1989). PubMed

Castoe TA et al. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc. Natl. Acad. Sci. U. S. A 110, 20645–50 (2013). PubMed PMC

Duan J et al. Transcriptome analysis of the response of Burmese python to digestion. Gigascience 6, 1–18 (2017). PubMed PMC

Gleeson TT, Mitchell GS & Bennett AF Cardiovascular responses to graded activity in the lizards Varanus and Iguana. Am. J. Physiol. Integr. Comp. Physiol 239, R174–R179 (1980). PubMed

Agaba M et al. Giraffe genome sequence reveals clues to its unique morphology and physiology. Nat. Commun 7, 11519 (2016). PubMed PMC

Weisenfeld NI, Kumar V, Shah P, Church DM & Jaffe DB Direct determination of diploid genome sequences. Genome Res 27, 757–767 (2017). PubMed PMC

Kichigin IG et al. Evolutionary dynamics of Anolis sex chromosomes revealed by sequencing of flow sorting-derived microchromosome-specific DNA. Mol. Genet. Genomics 291, 1955–1966 (2016). PubMed

Makunin AI et al. Contrasting origin of B chromosomes in two cervids (Siberian roe deer and grey brocket deer) unravelled by chromosome-specific DNA sequencing. BMC Genomics 17, 618 (2016). PubMed PMC

Martin M Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10 (2011).

Li H Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM (2013).

Quinlan AR & Hall IM BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–2 (2010). PubMed PMC

Quinlan AR, Pedersen BS & Dale RK Pybedtools: a flexible Python library for manipulating genomic datasets and annotations. Bioinformatics 27, 3423–3424 (2011). PubMed PMC

Kielbasa SM, Wan R, Sato K, Horton P & Frith M Adaptive seeds tame genomic sequence comparison. Genome Res (2011). doi:10.1101/gr.113985.110 PubMed DOI PMC

Kent WJ, Baertsch R, Hinrichs A, Miller W & Haussler D Evolution’s cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl. Acad. Sci 100, 11484–11489 (2003). PubMed PMC

Smit A, Hubley R & Green P Repeatmasker Open-4.0 (2013). Available at: http://www.repeatmasker.org. (Accessed: 10th January 2015)

Cantarel BL et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18, 188–96 (2008). PubMed PMC

Stanke M & Morgenstern B AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33, W465–7 (2005). PubMed PMC

Slater G & Birney E Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005). PubMed PMC

Dobin A et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013). PubMed PMC

Haas BJ et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc 8, 1494–512 (2013). PubMed PMC

Jones P et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014). PubMed PMC

Emms DM & Kelly S OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16, 157 (2015). PubMed PMC

Lowe TM & Eddy SR tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25, 955–64 (1997). PubMed PMC

Griffiths-Jones S, Bateman A, Marshall M, Khanna A & Eddy SR Rfam: an RNA family database. Nucleic Acids Res 31, 439–41 (2003). PubMed PMC

Nawrocki EP & Eddy SR Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–5 (2013). PubMed PMC

Löytynoja A Phylogeny-aware alignment with PRANK. in Methods in molecular biology (Clifton, N.J.) 1079, 155–170 (2014). PubMed

Nguyen LT, Schmidt HA, Von Haeseler A & Minh BQ IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol 32, 268–274 (2015). PubMed PMC

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A & Jermiin LS ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017). PubMed PMC

Hoang DT, Chernomor O, von Haeseler A, Minh BQ & Vinh LS UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol 35, 518–522 (2018). PubMed PMC

Smith SA, Brown JW & Walker JF So many genes, so little time: A practical approach to divergence-time estimation in the genomic era. PLoS One 13, e0197433 (2018). PubMed PMC

Han MV, Thomas GWC, Lugo-Martinez J & Hahn MW Estimating Gene Gain and Loss Rates in the Presence of Error in Genome Assembly and Annotation Using CAFE 3. Mol. Biol. Evol 30, 1987–1997 (2013). PubMed

Mitchell AL et al. InterPro in 2019: improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res (2018). doi:10.1093/nar/gky1100 PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ Basic local alignment search tool. J. Mol. Biol 215, 403–410 (1990). PubMed

Krogh A, Larsson B, von Heijne G & Sonnhammer EL. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen. J. Mol. Biol 305, 567–580 (2001). PubMed

Katoh K & Standley DM MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol 30, 772–780 (2013). PubMed PMC

Capella-Gutiérrez S, Silla-Martínez JM & Gabaldón T trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). PubMed PMC

Suyama M, Torrents D & Bork P PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34, (2006). PubMed PMC

Smith MD et al. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol. Biol. Evol 32, 1342–53 (2015). PubMed PMC

Pond SLK, Frost SDW & Muse SV HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676–679 (2005). PubMed

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