Abstract
The emerging field of phylogenomics considers genomic sequences under an evolutionary framework. We provide an overview of how different phylogenomic approaches can be used to address the study of fungal biology. This includes, among others, the establishment of the phylogenetic position of a newly sequenced species, the detection of past evolutionary events shaping a given genome, or the prediction of putative functions of uncharacterized proteins. Illustrative examples from recent work are provided along with pointers to useful tools and resources. Rather than a comprehensive treaty on fungal phylogenomics, our intention is to spark the interest of researchers considering the use of fungal genomic sequences but may not have considered exploiting a fully fledged phylogenomic approach.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Altincicek B, Kovacs JL, Gerardo NM (2011) Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Lett 8:253–257
Arvestad L, Berglund AC, Lagergren J, Sennblad B (2003) Bayesian gene/species tree reconciliation and orthology analysis using MCMC. Bioinformatics 19(Suppl 1):I7–I15
Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977
Berger AB, Cabal GG, Fabre E, Duong T, Buc H, Nehrbass U, Olivo-Marin JC, Gadal O, Zimmer C (2008) High-resolution statistical mapping reveals gene territories in live yeast. Nat Methods 5:1031–1037
Berglund AC, Sjolund E, Ostlund G, Sonnhammer EL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36:D263–D266
Bininda-Emonds OR (2005) Supertree construction in the genomic age. Methods Enzymol 395:745–757
Bullerwell CE, Leigh J, Forget L, Lang BF (2003) A comparison of three fission yeast mitochondrial genomes. Nucleic Acids Res 31:759–768
Bushley KE, Turgeon BG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10:26
Byrne KP, Wolfe KH (2006) Visualizing syntenic relationships among the hemiascomycetes with the Yeast Gene Order Browser. Nucleic Acids Res 34:D452–D455
Campbell MA, Rokas A, Slot JC (2012) Horizontal transfer and death of a fungal secondary metabolic gene cluster. Genome Biol Evol 4:289–293
Capella-Gutierrez S, Silla-Martinez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Capella-Gutierrez S, Marcet-Houben M, Gabaldon T (2012) Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10:47
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Cavalier-Smith T (1983) A six-kingdom classification and a unified phylogeny. In: Schenk HEA, Schwemmler W (eds) Endocytobiology II. de Gruyter, Berlin, pp 1027–1034
Creevey CJ, McInerney JO (2009) Trees from trees: construction of phylogenetic supertrees using CLANN. Methods Mol Biol 537:139–161
Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, Didier ES, Fan L, Heiman DI, Levin JZ, Young S, Zeng Q, Troemel ER (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22:2478–2488
de Juan D, Pazos F, Valencia A (2013) Emerging methods in protein co-evolution. Nat Rev Genet 14:249–261
Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375
Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113
Eirin-Lopez JM, Rebordinos L, Rooney AP, Rozas J (2012) The birth-and-death evolution of multigene families revisited. Genome Dyn 7:170–196
Eisen JA, Fraser CM (2003) Phylogenomics: intersection of evolution and genomics. Science 300:1706–1707
Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113
Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99
Fitzpatrick DA, O’Gaora P, Byrne KP, Butler G (2010) Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser. BMC Genomics 11:290
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Gorecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kues U, Kumar TK, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Duenas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719
Fraser JA, Huang JC, Pukkila-Worley R, Alspaugh JA, Mitchell TG, Heitman J (2005) Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot Cell 4:401–406
Gabaldón T (2005) Evolution of proteins and proteomes, a phylogenetics approach. Evol Bioinform Online 1:51–56
Gabaldón T (2008a) Comparative genomics-based prediction of protein function. Methods Mol Biol 439:387–401
Gabaldón T (2008b) Large-scale assignment of orthology: back to phylogenetics? Genome Biol 9:235
Gabaldón T, Huynen MA (2005) Lineage-specific gene loss following mitochondrial endosymbiosis and its potential for function prediction in eukaryotes. Bioinformatics 21(Suppl 2):ii144–ii150
Gabaldón T, Koonin EV (2013) Functional and evolutionary implications of gene orthology. Nat Rev Genet 14:360–366
Gabaldón T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 348:857–870
Gabaldón T, Marcet-Houben M, Huerta-Cepas J (2008) Reconstruction and analysis of large-scale phylogenetic data: challenges and opportunities. In: Russe A (ed) Computational biology: new research. Nova Science, New York, pp 129–146
Gill EE, Fast NM (2006) Assessing the microsporidia-fungi relationship: combined phylogenetic analysis of eight genes. Gene 375:103–109
Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274(546):563–567
Gojkovic Z, Knecht W, Zameitat E, Warneboldt J, Coutelis JB, Pynyaha Y, Neuveglise C, Moller K, Loffler M, Piskur J (2004) Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol Genet Genomics 271:387–393
Gribaldo S, Philippe H (2002) Ancient phylogenetic relationships. Theor Popul Biol 61:391–408
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Homouz D, Kudlicki AS (2013) The 3D organization of the yeast genome correlates with co-expression and reflects functional relations between genes. PLoS One 8:e54699
Huerta-Cepas J, Gabaldón T (2010) Assigning duplication events to relative temporal scales in genome-wide studies. Bioinformatics 27:38–45
Huerta-Cepas J, Dopazo H, Dopazo J, Gabaldón T (2007) The human phylome. Genome Biol 8:R109
Huerta-Cepas J, Dopazo J, Gabaldón T (2010) ETE: a python Environment for Tree Exploration. BMC Bioinformatics 11:24
Huerta-Cepas J, Capella-Gutierrez S, Pryszcz LP, Denisov I, Kormes D, Marcet-Houben M, Gabaldon T (2011) PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucleic Acids Res 39:D556–D560
Huynen MA, Bork P (1998) Measuring genome evolution. Proc Natl Acad Sci U S A 95:5849–5856
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lucking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–822
Jones MD, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, Richards TA (2011) Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474:200–203
Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453
Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64
Kaur R, Ma B, Cormack BP (2007) A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 104:7628–7633
Keeling PJ (2003) Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genet Biol 38:298–309
Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56:93–116
Khaldi N, Wolfe KH (2011) Evolutionary origins of the fumonisin secondary metabolite gene cluster in Fusarium verticillioides and Aspergillus niger. Int J Evol Biol 2011:423821
Kovalchuk A, Driessen AJ (2010) Phylogenetic analysis of fungal ABC transporters. BMC Genomics 11:177
Kristensen DM, Wolf YI, Mushegian AR, Koonin EV (2011) Computational methods for gene orthology inference. Brief Bioinform 12:379–391
Kriventseva EV, Rahman N, Espinosa O, Zdobnov EM (2008) OrthoDB: the hierarchical catalog of eukaryotic orthologs. Nucleic Acids Res 36:D271–D275
Landan G, Graur D (2007) Heads or tails: a simple reliability check for multiple sequence alignments. Mol Biol Evol 24:1380–1383
Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189
Liu Y, Leigh JW, Brinkmann H, Cushion MT, Rodriguez-Ezpeleta N, Philippe H, Lang BF (2009a) Phylogenomic analyses support the monophyly of Taphrinomycotina, including Schizosaccharomyces fission yeasts. Mol Biol Evol 26:27–34
Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF (2009b) Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9:272
Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, Abe A, Calvo SE, Corrochano LM, Engels R, Fu J, Hansberg W, Kim JM, Kodira CD, Koehrsen MJ, Liu B, Miranda-Saavedra D, O’Leary S, Ortiz-Castellanos L, Poulter R, Rodriguez-Romero J, Ruiz-Herrera J, Shen YQ, Zeng Q, Galagan J, Birren BW, Cuomo CA, Wickes BL (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5:e1000549
Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373
Marcet-Houben M, Gabaldon T (2009) The tree versus the forest: the fungal tree of life and the topological diversity within the yeast phylome. PLoS One 4:e4357
Marcet-Houben M, Gabaldon T (2010) Acquisition of prokaryotic genes by fungal genomes. Trends Genet 26:5–8
Marcet-Houben M, Marceddu G, Gabaldón T (2009) Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. BMC Evol Biol 9:295
Merhej V, Raoult D (2012) Rhizome of life, catastrophes, sequence exchanges, gene creations, and giant viruses: how microbial genomics challenges Darwin. Front Cell Infect Microbiol 2:113
Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627
Muller H, Thierry A, Coppee JY, Gouyette C, Hennequin C, Sismeiro O, Talla E, Dujon B, Fairhead C (2009) Genomic polymorphism in the population of Candida glabrata: gene copy-number variation and chromosomal translocations. Fungal Genet Biol 46:264–276
Notredame C (2007) Recent evolutions of multiple sequence alignment algorithms. PLoS Comput Biol 3:e123
Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217
Novakova E, Moran NA (2011) Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol 29:313–323
Ohno S (1970) Evolution by gene duplication. Allen & Unwin, London
Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P (2011) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40:D284–D289
Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650
Pryszcz L, Huerta-Cepas J, Gabaldón T (2011) MetaPhOrs: orthology and paralogy predictions from multiple phylogenetic evidence using a consistency-based confidence score. Nucleic Acids Res 39:e32
Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Sicheritz-Ponten T, Andersson SG (2001) A phylogenomic approach to microbial evolution. Nucleic Acids Res 29:545–552
Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38:1348–1354
Slot JC, Rokas A (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21:134–139
Snel B, Huynen MA, Dutilh BE (2005) Genome trees and the nature of genome evolution. Annu Rev Microbiol 59:191–209
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135
Van de Peer Y, Ben Ali A, Meyer A (2000) Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 246:1–8
Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Automatic genome-wide reconstruction of phylogenetic gene trees. Bioinformatics 23:i549–i558
Wehe A, Bansal MS, Burleigh JG, Eulenstein O (2008) DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony. Bioinformatics 24:1540–1541
Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713
Acknowledgments
We wish to thank all members of the Gabaldón group. Group research of T.G. is funded in part by a grant from the Spanish Ministry of Economy and Competitiveness (BIO2012-37161), a grant from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC (Grant Agreement n. ERC-2012-StG-310325), and a Grant from the Qatar National Research Fund grant (NPRP 5-298-3-086).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Gabaldón, T., Marcet-Houben, M. (2014). 3 Phylogenomics for the Study of Fungal Biology. In: Nowrousian, M. (eds) Fungal Genomics. The Mycota, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45218-5_3
Download citation
DOI: https://doi.org/10.1007/978-3-642-45218-5_3
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-45217-8
Online ISBN: 978-3-642-45218-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)