Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Powell, Amy J ^a   Conant, Gavin C ^b   Brown, Douglas E ^c   Carbone, Ignazio ^c   Dean, Ralph A ^c  

^a SANDIA NATIONAL LABORATORIES   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HYDROLASE; MELANIN; OXIDOREDUCTASE;

ARTICLE; ASCOMYCETES; BASIDIOMYCETES; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL GENETICS; FUNGAL VIRULENCE; GENE DUPLICATION; GENE FUNCTION; GENETIC CODE; HORMONE SYNTHESIS; HOST CELL; MULTIGENE FAMILY; NONHUMAN; PREDICTION; SPECIES DIFFERENCE; BIOLOGY; COMPARATIVE STUDY; FUNGUS; GENETICS; GENOMICS; MOLECULAR EVOLUTION; PATHOGENICITY; SEQUENCE HOMOLOGY;

FUNGI;

COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; FUNGI; GENE DUPLICATION; GENOMICS; MULTIGENE FAMILY; SEQUENCE HOMOLOGY;

EID: 42549135491     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-147     Document Type: Article

References (99)

1. Welch RA Burland V Plunkett G Redford P Roesch P Rasko D Buckles EL Liou SR Boutin A Hackett J Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli Proceedings of the National Academy of Sciences of the United States of America 2002, 99(26):17020-17024. 12471157 10.1073/pnas.252529799 139262
2. Holden MTG Feil EJ Lindsay JA Peacock SJ Day NPJ Enright MC Foster TJ Moore CE Hurst L Atkin R Complete genomes of two clinical Staphylococcus aureus strains: Evidence for the rapid evolution of virulence and drug resistance Proceedings of the National Academy of Sciences of the United States of America 2004, 101(26):9786-9791. 15213324 10.1073/ pnas.0402521101 470752
3. Hacker J Carniel E Ecological fitness, genomic islands and bacterial pathogenicity - A Darwinian view of the evolution of microbes EMBO reports 2001, 2(5):376-381. 1083891 11375927
4. Heidelberg JF Eisen JA Nelson WC Clayton RA Gwinn ML Dodson RJ Haft DH Hickey EK Peterson JD Umayam L DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae Nature 2000, 406(6795):477-483. 10952301 10.1038/35020000
5. McLysaght A Baldi PF Gaut BS Extensive gene gain associated with adaptive evolution of poxviruses Proceedings of the National Academy of Sciences of the United States of America 2003, 100(26):15655-15660. 14660798 10.1073/pnas.2136653100 307623
6. Hughes AL Friedman R Poxvirus genome evolution by gene gain and loss Molecular Phylogenetics and Evolution 2005, 35(1):186-195. 10.1016/ j.ympev.2004.12.008
7. Parkhill J Wren BW Thomson NR Titball RW Holden MTG Prentice MB Sebaihia M James KD Churcher C Mungall KL Genome sequence of Yersinia pestis, the causative agent of plague Nature 2001, 413(6855):523-527. 11586360 10.1038/35097083
8. Lawrence JG Common themes in the genome strategies of pathogens Current Opinion in Genetics and Development 2005, 15:584-588. 10.1016/ j.gde.2005.09.007
9. Hane JK Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum Personal communication 2007.
10. Dean RA Talbot NJ Ebbole DJ Farman ML Mitchell TK Orbach MJ Thon M Kulkarni R Xu JR Pan HQ The genome sequence of the rice blast fungus Magnaporthe grisea Nature 2005, 434(7036):980-986. 15846337 10.1038/ nature03449
11. Cuomo CA Gueldener U Xu JR Trail F Turgeon BG Di Pietro A Walton JD Ma LJ Baker SE Rep M The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization Science 2007, 317(5843):1400-1402. 17823352 10.1126/science.1143708
12. Martinez D Genome sequence analysis of the cellulolytic fungus Trichoderma reesei (syn. Hypocrea jecorina) reveals a surprisingly limited inventory of carbohydrate active enzymes Personal communication 2007.
13. Tyler BM Tripathy S Zhang XM Dehal P Jiang RHY Aerts A Arredondo FD Baxter L Bensasson D Beynon JL Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis Science 2006, 313(5791):1261-1266. 16946064 10.1126/science.1128796
14. Armbrust EV Berges JA Bowler C Green BR Martinez D Putnam NH Zhou SG Allen AE Apt KE Bechner M The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism Science 2004, 306(5693):79-86. 15459382 10.1126/science.1101156
15. Galagan JE Calvo SE Borkovich KA Selker EU Read ND Jaffe D FitzHugh W Ma LJ Smirnov S Purcell S The genome sequence of the filamentous fungus Neurospora crassa Nature 2003, 422(6934):859-868. 12712197 10.1038/ nature01554
16. Machida M Asai K Sano M Tanaka T Kumagai T Terai G Kusumoto KI Arima T Akita O Kashiwagi Y Genome sequencing and analysis of Aspergillus oryzae Nature 2005, 438(7071):1157-1161. 16372010 10.1038/nature04300
17. Payne GA Nierman WC Wortman JR Pritchard BL Brown D Dean RA Bhatnagar D Cleveland TE Machida M Yu J Whole genome comparison of Aspergillus flavus and A. oryzae Medical Mycology 2006, 44:S9-S11. 10.1080/ 13693780600835716
18. Kamper J Kahmann R Bolker M Ma LJ Brefort T Saville BJ Banuett F Kronstad JW Gold SE Muller O Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis Nature 2006, 444(7115):97-101. 17080091 10.1038/nature05248
19. Egan MJ Wang ZY Jones MA Smirnoff N Talbot NJ Generation of reactive oxygen species by fungal NADPH oxidases is required for the rice blast disease PNAS 2007, 104(28):11772-11777. 17600089 10.1073/pnas.0700574104 1913907
20. Tosa Y Osue J Eto Y Oh HS Nakayashiki H Mayama S Leong SA Evolution of an avirulence gene AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae Molecular Plant-Microbe Interactions 2005, 18(11):1148-1160. 16353550 10.1094/MPMI-18-1148
21. Win J Morgan W Bos J Krasileva KV Cano LM Chaparro-Garcia A Ammar R Staskawicz BJ Kamoun S Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic Oomycetes The Plant Cell 2007. 17675403
22. Deng JX Carbone I Dean RA The evolutionary history of Cytochrome P450 genes in four filamentous Ascomycetes BMC Evolutionary Biology 2007, 7:30. 17324274 10.1186/1471-2148-7-30 1828051
23. Keon J Antoniw J Carzaniga R Deller S Ward JL Baker JM Beale MH Hammond-Kosack K Rudd JJ Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible host Molecular Plant-Microbe Interactions 2007, 20(2):178-193. 17313169 10.1094/MPMI-20-2-0178
24. Kroken S Glass NL Taylor JW Yoder OC Turgeon GB Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascyomycetes PNAS 2003, 100(26):15670-15675. 14676319 10.1073/pnas.2532165100 307626
25. Braun BR Hoog MV d'Enfert C Martchenko M Dungan J Kuo A Inglis DO Uhl MA Hogues H Berriman M A human-curated annotation of the Candida albicans genome PLOS Genetics 2005, 1(1):36-57. 16103911 10.1371/ journal.pgen.0010001 1183520
26. Xu JR Peng YL Dickman MB Sharon A The dawn of fungal pathogen genomics Annual Review of Phytopathology 2006, 44:337-366. 16704358 10.1146/ annurev.phyto.44.070505.143412
27. Jordan IK Makarova KS Spouge JL Wolf YI Koonin EV Lineage-specific gene expansions in Bacterial and Archaeal genomes Genome Research 2001, 11:555-565. 11282971 10.1101/gr.GR-1660R 311027
28. Lespinet O Wolf YI Koonin EV Aravind L The role of lineage-specific gene family expansion in the evolution of Eukaryotes Genome Research 2002, 12:1048-1059. 12097341 10.1101/gr.174302 186617
29. Kulkarni RD Thon MR Pan HQ Dean RA Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea Genome Biology 2005, 6:3. 1088943 15774025
30. Skamnioti P Gurr SJ Magnaporthe grisea Cutinase2 Mediates Appressorium Differentiation and Host Penetration and Is Required for Full Virulence The Plant Cell 2007. 2002628 17704215
31. Carbone I Jakobek JL Ramirez-Prado JH Horn BW Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus Molecular Ecology 2007, 16:4401-4417. 17725568 10.1111/j.1365-294X.2007.03464.x
32. Carbone I Ramirez-Prado JH Jakobek JL Horn BW Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster BMC Evolutionary Biology 2007, 7:111. 17620135 10.1186/1471-2148-7-111 1949824
33. Hotopp JCD Widespread lateral gene transfer from intracellular Bacteria to multicellular Eukaryotes Science 2007, 317:1753-1756. 17761848 10.1126/science.1142490
34. Friesen TL Stuckenbrock EH Liu Z Meinhardt S Ling H Faris JD Rasmussen JB Solomon PS McDonald BA Oliver RP Emergence of a new disease as a result of interspecific virulence gene transfer Nature Genetics 2006, 38(8):953-956. 16832356 10.1038/ng1839
35. Paoletti M Buck KW Braiser CM Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi Molecular Ecology 2006, 15(1):249-262. 16367844 10.1111/j.1365-294X.2005.02728.x
36. Galagan JE Henn MR Ma LJ Cuomo CA Birren B Genomics of the fungal kingdom: Insights into eukaryotic biology Genome Research 2005, 15(12):1620-1631. 16339359 10.1101/gr.3767105
37. Galagan JE Calvo SE Cuomo C Ma LJ Wortman JR Batzoglou S Lee SI Basturkmen M Spevak CC Clutterbuck J Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae Nature 2005, 438(7071):1105-1115. 16372000 10.1038/nature04341
38. Loftus BJ Fung E Roncaglia P Rowley D Amedeo P Bruno D Vamathevan J Miranda M Anderson IJ Fraser JA The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans Science 2005, 307(5713):1321-1324. 15653466 10.1126/science.1103773
39. Katinka MD Duprat S Cornillot E Metenier G Thomarat F Prensier G Barbe V Peyretaillade E Brottier P Wincker P Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Nature 2001, 414(6862):450-453. 11719806 10.1038/35106579
40. Nierman WC Pain A Anderson MJ Wortman JR Kim HS Arroyo J Berriman M Abe K Archer DB Bermejo C Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus Nature 2006, 439(7075):502-502. 10.1038/nature04572
41. Sachs JL Bull JJ Experimental evolution of conflict mediation between genomes PNAS 2005, 102(2):390-395. 15630098 10.1073/pnas.0405738102 544279
42. McDowell JM Simon SA Recent insights into R gene evolution Molecular Plant Pathology 2006, 7(5):437-448. 10.1111/j.1364-3703.2006.00342.x
43. Clay K Kover PX The Red Queen hypothesis and plant/pathogen interactions Annu Rev Phytopathol 1996, 34:29-50. 15012533 10.1146/ annurev.phyto.34.1.29
44. Huynen MA van Nimwegen E The frequency distribution of gene family sizes in complete genomes Mol Bio Evol 1998, 15(5):583-589.
45. Reed WJ Hughes BD A model explaining the size distribution of gene and protein families Mathematical Biosciences 2004, 189(1):97-102. 15051416 10.1016/j.mbs.2003.11.002
46. Koonin EV Wolf YI Karev GP The structure of the protein universe and genome evolution Nature 2002, 420(6912):218-223. 12432406 10.1038/ nature01256
47. Koonin EV Wolf YI Karev GP Power laws, scale-free networks and genome biology Georgetown, Tex. & New York, N.Y.: Landes Bioscience/ Eurekah.com; Springer Science+Business Media 2006.
48. Fitzpatrick DA Logue ME Stajich JE Butler G A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis BMC Evolutionary Biology 2006:6.
49. James TY Kauff F Schoch CL Matheny PB Hofstetter V Cox CJ Celio G Gueidan C Fraker E Miadlikowska J Reconstructing the early evolution of Fungi using a six-gene phylogeny Nature 2006, 443(7113):818-822. 17051209 10.1038/nature05110
50. Sidhu GS Mycotoxin genetics and gene clusters European Journal of Plant Pathology 2002, 108:705-711. 10.1023/A:1020613413483
51. Keller NP Turner G Bennett JW Fungal secondary metabolism-from biochemistry to genomics Nature Reviews: Microbiology 2005, 3:937-947. 16322742 10.1038/nrmicro1286
52. Bok JW Keller NP LaeA, a regulator of secondary metabolism in Aspergillus species Eukaryotic Cell 2004, 3(2):527-535. 15075281 10.1128/ EC.3.2.527-535.2004 387652
53. Costanzo S Ospina-Giraldo MD Deahl KL Baker CJ Jones RW Gene duplication event in family 12 glycosyl hydrolase from Phytophthora spp Fungal Genetics and Biology 2006, 43:707-714. 10.1016/j.fgb.2006.04.006
54. Wolfe KH Comparative genomics and genome evolution in yeasts Philosophical Transactions of The Royal Society 2006, 361(1467):403-412. 10.1098/rstb.2005.1799
55. Berbee ML The phylogeny of plant and animal pathogens in the Ascomycota Physiological and Molecular Plant Pathology 2001, 59:165-187. 10.1006/ pmpp.2001.0355
56. Galagan JE Selker EU RIP: The evolutionary cost of genome defense Trends in Genetics 2004, 20(9):417-423. 15313550 10.1016/j.tig.2004.07.007
57. Ikeda K Nakayashiki H Kataoka T Tamba H Hashimoto Y Tosa Y Mayama S Repeat-induced point mutation (RIP) in Magnaporthe grisea: Implications for its sexual: Cycle in the natural field context Molecular Microbiology 2002, 45(5):1355-1364. 12207702 10.1046/ j.1365-2958.2002.03101.x
58. Montiel MD Lee HA Archer DB Evidence of RIP (repeat-induced point mutation) in transposase sequences of Aspergillus oryzae Fungal Genetics and Biology 2006, 43:439-445. 10.1016/j.fgb.2006.01.011
59. Faugeron G Diversity of homology-dependent gene silencing strategies in fungi Current Opinion in Microbiology 2000, 3(2):144-148. 10744998 10.1016/S1369-5274(00)00066-7
60. Martinez D Larrondo LF Putnam N Gelpke MDS Huang K Chapman J Helfenbein KG Ramaiya P Detter JC Larimer F Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 Nature Biotechnology 2004, 22(6):695-700. 15122302 10.1038/nbt967
61. Hood ME Katawczik M Giraud T Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum Genetics 2005, 170:1081-1089. 15911572 10.1534/genetics.105.042564 1451165
62. Berbee ML Taylor JW Dating divergences in the fungal tree of life: Review and new analyses Mycologia 2006, 98(6):838-849. 17486961
63. Berbee ML Taylor JW Fungal molecular evolution: Gene trees and geologic time The Mycota VII Part B: Systematics and Evolution 2001:229-245.
64. St Leger RJ Joshi L Roberts DW Adaptation of proteases and carbohydrases of saprophytic, phytopathogenic and entomopathogenic fungi to the requirements of their ecological niches Microbiology 1997, 143(6):1983-1992. 9202474
65. Rappleye CA Goldman WE Defining virulence genes in the dimorphic fungi Annu Rev Microbiol 2006, 60:281-303. 16753032 10.1146/ annurev.micro.59.030804.121055
66. Sexton AC Howlett BJ Parallels in fungal pathogenesis on plant and animal hosts Eukaryotic Cell 2006, 5(12):1941-1949. 17041185 10.1128/ EC.00277-06 1694825
67. Xu J Zhao X Dean RA Jay CD From Genes to Genomes: A New Paradigm for Studying Fungal Pathogenesis in Magnaporthe oryzae Advances in genetics Academic Press 2007, 57:175-218. 17352905
68. Lindstrom JT Belanger FC Purification and characterization of an endophytic fungal proteinase that is abundantly expressed in the infected host grass Plant Physiology 1994, 106:7-16. 159493 12232300
69. Reddy PV LCK Belanger FC Mutualistic Fungal Endophytes Express a Proteinase that Is Homologous to Proteases Suspected to Be Important in Fungal Pathogenicity Plant Physiology 1996, 111(4):1209-1218. 8756501 10.1104/pp.111.4.1209 160998
70. Nahar P Ghormade V Deshpande MV The extracellular constitutive production of chitin deacetylase in Metarhizium anisopliae: Possible edge to entomopathogenic fungi in the biological control of insect pests Journal of Invertebrate Pathology 2004, 85(2):80-88. 15050837 10.1016/ j.jip.2003.11.006
71. Lee BN Kroken S Chou DYT Robbertse B Yoder OC Turgeon BG Functional Analysis of All Nonribosomal Peptide Synthetases in Cochliobolus heterostrophus Reveals a Factor, NPS6, Involved in Virulence and Resistance to Oxidative Stress Eukaryotic Cell 2005, 4(3):545-555. 15755917 10.1128/EC.4.3.545-555.2005 1087798
72. Cary JW OBrian GR Nielsen DM Nierman W Harris-Coward P Yu J Bhatnagar D Cleveland TE Payne GA Calvo AM Elucidation of veA- dependent genes associated with aflatoxin and sclerotial production in Aspergillus flavus by functional genomics Applied Microbiology and Biotechnology 2007.
73. Wolfe KH Shields DC Molecular evidence for an ancient duplication of the entire yeast genome Nature 1997, 387(6634):708-713. 9192896 10.1038/42711
74. Conant GC Wolfe KH Increased glycolytic flux as an outcome of whole-genome duplication in yeast Molecular Systems Biology 2007, 3:129. 17667951 10.1038/msb4100170 1943425
75. Talbot NJ On the trail of a cereal killer: Exploring the Biology of Magnaporthe grisea Annu Rev Microbiol 2003, 57:177-202. 14527276 10.1146/ annurev.micro.57.030502.090957
76. Halaouli S Asther M Sigoillot JC Hamdi M Lomascolo A Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications Journal of Applied Microbiology 2006, 100:219-232. 16430498 10.1111/j.1365-2672.2006.02866.x
77. Thompson JE Basarab GS Andersson A Lindqvist Y Jordan DB Trihydroxynaphthalene Reductase from Magnaporthe grisea: Realization of an Active Center Inhibitor and Elucidation of the Kinetic Mechanism Biochemistry 1996, 36(7):1852-1860. 10.1021/bi962355u
78. McPherson MJ Ogel ZB Stevens C Yadav KDS Keen JN Knowles PF Galatose oxidase of Dactylium dendroides The Journal of Biological Chemistry 1992, 267(12):8146-8152. 1569070
79. Rolke Y Liu S Quidde T Williamson B Schouten A Weltring KM Siewers V Tenberge KB Tudzynski B Tudzynski P Functional analysis of H2O2-generating systems in Botrytis cinerea: The major Cu-Zn-superoxide dismutase (BCSOD1) contributes to virulence on french bean, whereas a glucose oxidase (BCGOD1) is dispensable Molecular Plant Pathology 2004, 5(1):17-27. 10.1111/j.1364-3703.2004.00201.x
80. Wolfe KH Li WH Molecular evolution meets the genomics revolution Nature Genetics Supplement 2003, 33:255-265. 10.1038/ng1088
81. Lynch M O'Hely M Walsh B Force A The probability of preservation of a newly arisen gene duplicate Genetics 2001, 159(4):1789-1804. 1461922 11779815
82. Conant GC Wagner A GenomeHistory: A software tool and its application to fully sequenced genomes Nucleic Acids Research 2002, 30(15):3378-3386. 12140322 10.1093/nar/gkf449 137074
83. Fungal Genome Initiative http://www.broad.mit.edu/annotation/fungi/fgi/
84. Eukaryotic Genomics http://genome.jgi-psf.org/
85. Entrez Genome http://www.ncbi.nlm.nih.gov/sites/entrez?db=genome
86. Aspergillus oryzae genome http://www.bio.nite.go.jp/dogan/ MicroTop?GENOME_ID=ao
87. Repbase http://www.girinst.org/
88. Jurka J Kapitonov VV Pavlicek A Klonowski P Kohany O Walichiewicz J Repbase Update, a database of Eukaryotic repetitive elements Cytogenetic and Genome Research 2005, 110:462-467. 10.1159/000084979
89. Brown DE Powell AJ Carbone I Dean RA GT-Miner: A graph-theoretic data miner, viewer and model processor Personal communication 2008.
90. Chartrand G Oellermann OR Applied and Algorithmic Graph Theory New York: McGraw-Hill 1993.
91. Bollobas B Graph Theory: An introductory Course Heidelberg: Springer-Verlag 1979.
92. Press WH Flannery BP Teukolsky SA Vetterling WT Numerical Recipes in C: the art of scientific computing Cambridge; New York: Cambridge University Press second 1992.
93. Sokal RR Rohlf FJ Biometry WH Freeman and Company, New York Third 1995. ISBN-10: 0716724111
94. The Gene Ontology database http://www.geneontology.org/ GO.downloads.database.shtml
95. The Gene OC The Gene Ontology (GO) database and informatics resource Nucleic Acids Research 2004, 32 Database:D258-D261. 308770 14681407
96. Cai Z Mao X Li S Wei L Genome comparison using Gene Ontology (GO) with statistical testing BMC Bioinformatics 2006.
97. The Gene OC GO Slim http://www.geneontology.org/GO.slims.shtml
98. Benjamini Y Hochberg Y Controlling the false discovery rate: A practical and powerful approach to multiple testing Journal of the Royal Statistical Society 1995, 57(1):289-300.
99. Altschul SF Madden TL Schaffer AA Zhang J Zhang Z Miller W Lipman DJ Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res 1997, 25(17):3389-3402. 9254694 10.1093/nar/ 25.17.3389 146917