Identification of horizontally transferred genes in the genus Colletotrichum reveals a steady tempo of bacterial to fungal gene transfer

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Jaramillo, Armijos D ^a   Sukno, Serenella A ^a   Thon, Michael R ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Anthracnose; Bacteria; Colletotrichum; Horizontal gene transfer; Molecular clock; Pezizomycotina; Phytopathogen

Indexed keywords

ARTICLE; ASCOMYCETES; COLLETOTRICHUM; CONTROLLED STUDY; FUNGAL GENOME; GENE DUPLICATION; GENE IDENTIFICATION; GENE LOSS; GLOMERELLA GRAMINICOLA; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; NONHUMAN; PEZIZOMYCOTINA; PHYLOGENETIC TREE; BACTERIAL GENE; BACTERIUM; FUNGAL GENE; GENE DELETION; GENETICS; PHYLOGENY; PHYSIOLOGY; PROTEIN DATABASE;

BACTERIA (MICROORGANISMS); COLLETOTRICHUM; EUKARYOTA; FUNGI; PEZIZOMYCOTINA; PROKARYOTA;

BACTERIA; COLLETOTRICHUM; DATABASES, PROTEIN; GENE DELETION; GENE DUPLICATION; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENES, FUNGAL; PHYLOGENY;

EID: 84924285907     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-16-2     Document Type: Article

References (88)

1. Rosewich UL, Kistler HC: Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 2000, 38: 325-363. 10.1146/annurev.phyto.38.1.325
2. Koonin EV, Wolf YI: Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 2008, 36: 6688-6719. 10.1093/nar/gkn668
3. Wolf YI, Makarova KS, Yutin N, Koonin EV: Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol Direct 2012, 7: 46. 10.1186/1745-6150-7-46
4. Borziak K, Fleetwood AD, Zhulin IB: Chemoreceptor gene loss and acquisition via horizontal gene transfer in Escherichia coli. J Bacteriol 2013, 195: 3596-3602. 10.1128/JB.00421-13
5. Kitahara K, Miyazaki K: Revisiting bacterial phylogeny: natural and experimental evidence for horizontal gene transfer of 16S rRNA. Mob Genet Elem 2013, 3: e24210. 10.4161/mge.24210
6. Schaack S, Gilbert C, Feschotte C: Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 2010, 25: 537-546. 10.1016/j.tree.2010.06.001
7. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim W-B, Woloshuk C, Xie X, Xu J-R, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RAE, Chapman S, Coulson R, Coutinho PM, Danchin EGJ, Diener A, Gale LR, Gardiner DM, Goff S, et al.: Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464: 367-373. 10.1038/nature08850
8. Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M'barek S, Gohari AM, Jashni MK, Stergiopoulos I, Kema GHJ, de Wit PJGM: Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 2011, 35: 542-554. 10.1111/j.1574-6976.2010.00263.x
9. Milani NA, Lawrence DP, Arnold AE, VanEtten HD: Origin of pisatin demethylase (PDA) in the genus Fusarium. Fungal Genet Biol 2012, 49: 933-942. 10.1016/j.fgb.2012.08.007
10. Sun B-F, Xiao J-H, He S, Liu L, Murphy RW, Huang D-W: Multiple interkingdom horizontal gene transfers in Pyrenophora and closely related species and their contributions to phytopathogenic lifestyles. PLoS One 2013, 8: e60029. 10.1371/journal.pone.0060029
11. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ: Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 2006, 16: 1857-1864. 10.1016/j.cub.2006.07.052
12. Richards TA, Leonard G, Soanes DM, Talbot NJ: Gene transfer into the fungi. Fungal Biol Rev 2011, 25: 98-110. 10.1016/j.fbr.2011.04.003
13. Irelan JT, Selker EU: Gene silencing in filamentous fungi: RIP, MIP and quelling. J Genet 1996, 75: 313-324. 10.1007/BF02966311
14. Richards TA, Hirt RP, Williams BAP, Embley TM: Horizontal gene transfer and the evolution of parasitic protozoa. Protist 2003, 154: 17-32. 10.1078/143446103764928468
15. Keeling PJ, Palmer JD: Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 2008, 9: 605-618. 10.1038/nrg2386
16. Fitzpatrick DA: Horizontal gene transfer in fungi. FEMS Microbiol Lett 2011, 329:1-8.
17. Griffiths AJ: Natural plasmids of filamentous fungi. Microbiol Rev 1995, 59:673-685.
18. Doolittle WF: You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 1998, 14: 307-311. 10.1016/S0168-9525(98)01494-2
19. Friesen TL, Stukenbrock 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. Nat Genet 2006, 38: 953-956. 10.1038/ng1839
20. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ: Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 2009, 21: 1897-1911. 10.1105/tpc.109.065805
21. Slot JC, Rokas A: Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc Natl Acad Sci U S A 2010, 107: 10136-10141. 10.1073/pnas.0914418107
22. Azad RK, Lawrence JG: Detecting laterally transferred genes. Methods Mol Biol 2012, 855: 281-308. 10.1007/978-1-61779-582-4_10
23. Brown JR: Ancient horizontal gene transfer. Nat Rev Genet 2003, 4: 121-132. 10.1038/nrg1000
24. Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD: The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 2012, 13: 414-430. 10.1111/j.1364-3703.2011.00783.x
25. Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW, Damm U, Goodwin PH, Chen H, Johnston PR, Jones EBG: Colletotrichum -names in current use. Fungal Divers 2009, 39:147.
26. Prusky D, Freeman S, Dickman MB: Colletotrichum: Host Specificity, Pathology, and Host-Pathogen Interaction. United States of America: American Phytopathological Society (APS Press). 2000.
27. Sukno SA, García VM, Shaw BD, Thon MR: Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl Environ Microbiol 2008, 74: 823-832. 10.1128/AEM.01165-07
28. Thon M, Nuckles E, Takach J, Vaillancourt L: CPR1: a gene encoding a putative signal peptidase that functions in pathogenicity of Colletotrichum graminicola to maize. Mol Plant-Microbe Interact 2002, 15: 120-128. 10.1094/MPMI.2002.15.2.120
29. Vargas WA, Martín JMS, Rech GE, Rivera LP, Benito EP, Díaz-Mínguez JM, Thon MR, Sukno SA: Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotrichum graminicola in maize. Plant Physiol 2012, 158: 1342-1358. 10.1104/pp.111.190397
30. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmüller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun M-H, et al.: Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 2012, 44: 1060-1065. 10.1038/ng.2372
31. Gan P, Ikeda K, Irieda H, Narusaka M, O'Connell RJ, Narusaka Y, Takano Y, Kubo Y, Shirasu K: Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 2013, 197: 1236-1249. 10.1111/nph.12085
32. Alkan N, Meng X, Friedlander G, Reuveni E, Sukno S, Sherman A, Thon M, Fluhr R, Prusky D: Global aspects of pacC regulation of pathogenicity genes in Colletotrichum gloeosporioides as revealed by transcriptome analysis. Mol Plant Microbe Interact 2013, 26: 1345-1358. 10.1094/MPMI-03-13-0080-R
33. Armijos Jaramillo VD, Vargas WA, Sukno SA, Thon MR: Horizontal transfer of a subtilisin gene from plants into an ancestor of the plant pathogenic fungal genus Colletotrichum. PLoS One 2013, 8: e59078. 10.1371/journal.pone.0059078
34. Marcet-Houben M, Gabaldón T: Acquisition of prokaryotic genes by fungal genomes. Trends Genet 2010, 26: 5-8. 10.1016/j.tig.2009.11.007
35. Schomburg I, Chang A, Placzek S, Söhngen C, Rother M, Lang M, Munaretto C, Ulas S, Stelzer M, Grote A, Scheer M, Schomburg D: BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res 2013,41(Database issue):D764-D772.
36. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M: KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012,40(Database issue):D109-D114.
37. Caspi R, Altman T, Dale JM, Dreher K, Fulcher CA, Gilham F, Kaipa P, Karthikeyan AS, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Paley S, Popescu L, Pujar A, Shearer AG, Zhang P, Karp PD: The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 2010,38(suppl 1):D473-D479.
38. Rawlings ND, Barrett AJ, Bateman A: MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2011, 40:D343-D350.
39. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B: The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2013, 42:D490-D495.
40. Jogl G, Hsiao Y-S, Tong L: Structure and function of carnitine acyltransferases. Ann N Y Acad Sci 2004, 1033: 17-29. 10.1196/annals.1320.002
41. Zhao Z, Liu H, Wang C, Xu J-R: Correction: comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2014, 15: 6. 10.1186/1471-2164-15-6
42. Smith K, Nadeau K, Bradley M, Walsh C, Fairlamb AH: Purification of glutathionylspermidine and trypanothione synthetases from Crithidia fasciculata. Protein Sci 1992, 1: 874-883. 10.1002/pro.5560010705
43. Chiang B-Y, Chen T-C, Pai C-H, Chou C-C, Chen H-H, Ko T-P, Hsu W-H, Chang C-Y, Wu W-F, Wang AH-J, Lin C-H: Protein S-thiolation by glutathionylspermidine (Gsp): the role of escherichia coli Gsp synthetASE/amidase in redox regulation. J Biol Chem 2010, 285: 25345-25353. 10.1074/jbc.M110.133363
44. Zhao Z, Liu H, Wang C, Xu J-R: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2013, 14: 274. 10.1186/1471-2164-14-274
45. Van Vu B, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H: Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant Microbe Interact 2012, 25: 1135-1141. 10.1094/MPMI-02-12-0043-R
46. Inderbitzin P, Asvarak T, Turgeon BG: Six new genes required for production of T-toxin, a polyketide determinant of high virulence of Cochliobolus heterostrophus to maize. Mol Plant Microbe Interact 2010, 23: 458-472. 10.1094/MPMI-23-4-0458
47. Yasmin S, Alcazar-Fuoli L, Gründlinger M, Puempel T, Cairns T, Blatzer M, Lopez JF, Grimalt JO, Bignell E, Haas H: Mevalonate governs interdependency of ergosterol and siderophore biosyntheses in the fungal pathogen Aspergillus fumigatus. Proc Natl Acad Sci U S A 2012, 109: E497-E504. 10.1073/pnas.1106399108
48. Namiki F, Matsunaga M, Okuda M, Inoue I, Nishi K, Fujita Y, Tsuge T: Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol Plant Microbe Interact 2001, 14: 580-584. 10.1094/MPMI.2001.14.4.580
49. Wapinski I, Pfeffer A, Friedman N, Regev A: Natural history and evolutionary principles of gene duplication in fungi. Nature 2007, 449: 54-61. 10.1038/nature06107
50. Taylor TN, Hass H, Kerp H, Krings M, Hanlin RT: Perithecial Ascomycetes from the 400 million year old rhynie chert: an example of ancestral polymorphism. Mycologia 2005, 97: 269-285. 10.3852/mycologia.97.1.269
51. Garcia-Vallvé S, Romeu A, Palau J: Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 2000, 17: 352-361. 10.1093/oxfordjournals.molbev.a026315
52. Schmitt I, Lumbsch HT: Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 2009, 4: e4437. 10.1371/journal.pone.0004437
53. Takahara H, Huser A, O'Connell R: Two arginine biosynthesis genes are essential for pathogenicity of Colletotrichum higginsianum on Arabidopsis. Mycology 2012, 3:54-64.
54. Boggs JM, South AH, Hughes AL: Phylogenetic analysis supports horizontal gene transfer of L-amino acid oxidase gene in Streptococcus oligofermentans. Infect Genet Evol 2012, 12: 1005-1009. 10.1016/j.meegid.2012.02.014
55. Marri PR, Hao W, Golding GB: The role of laterally transferred genes in adaptive evolution. BMC Evol Biol 2007,7(Suppl 1):S8. 10.1186/1471-2148-7-S1-S8
56. Rohmer L, Hocquet D, Miller SI: Are pathogenic bacteria just looking for food? metabolism and microbial pathogenesis. Trends Microbiol 2011, 19: 341-348. 10.1016/j.tim.2011.04.003
57. Soanes D, Richards TA: Horizontal gene transfer in eukaryotic plant pathogens. Annu Rev Phytopathol 2014, 52: 583-614. 10.1146/annurev-phyto-102313-050127
58. Altschul SF, Madden TL, Schäffer 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: 3389-3402. 10.1093/nar/25.17.3389
59. Katoh K, Misawa K, Kuma K, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 2002, 30: 3059-3066. 10.1093/nar/gkf436
60. Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56: 564-577. 10.1080/10635150701472164
61. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59: 307-321. 10.1093/sysbio/syq010
62. Moreira D, Philippe H: Molecular phylogeny: pitfalls and progress. Int Microbiol 2000, 3:9-16.
63. Rech G PhD tesis. In Insight into the evolution of a plant pathogen: comparative genomic analysis of the fungal maize pathogen Colletotrichum graminicola. Universidad de Salamanca, Departamento de microbiología y genética. 2013.
64. Hendy MD, Penny D: A framework for the quantitative study of evolutionary trees. Syst Biol 1989, 38:297-309.
65. Ronquist F, Huelsenbeck JP: MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180
66. Notredame C, Higgins DG, Heringa J: T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302: 205-217. 10.1006/jmbi.2000.4042
67. Pruitt KD, Tatusova T, Brown GR, Maglott DR: NCBI reference sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 2012, 40: D130-D135. 10.1093/nar/gkr1079
68. Kohany O, Gentles AJ, Hankus L, Jurka J: Annotation, submission and screening of repetitive elements in repbase: RepbaseSubmitter and censor. BMC Bioinforma 2006, 7: 474. 10.1186/1471-2105-7-474
69. Stöver BC, Müller KF: TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinforma 2010, 11: 7. 10.1186/1471-2105-11-7
70. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21: 3674-3676. 10.1093/bioinformatics/bti610
71. Zdobnov EM, Apweiler R: InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17: 847-848. 10.1093/bioinformatics/17.9.847
72. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K: WoLF PSORT: protein localization predictor. Nucleic Acids Res 2007,35(Web Server):W585-W587. 10.1093/nar/gkm259
73. Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8: 785-786. 10.1038/nmeth.1701
74. Winnenburg R, Urban M, Beacham A, Baldwin TK, Holland S, Lindeberg M, Hansen H, Rawlings C, Hammond-Kosack KE, Köhler J: PHI-base update: additions to the pathogen host interaction database. Nucleic Acids Res 2008,36(Database issue):D572-D576.
75. Chen L, Xiong Z, Sun L, Yang J, Jin Q: VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 2012,40(Database issue):D641-D645.
76. Lu T, Yao B, Zhang C: DFVF: database of fungal virulence factors. Database (Oxford) 2012, 2012:bas032.
77. R Development Core Team: R: A Language and Environment for Statistical Computing. R. Vienna, Austria: R Foundation for Statistical Computing. 2011.
78. Peden JF Ph.D Thesis. In Analysis of Codon Usage. University of Nottingham. 1999.
79. Marthey S, Aguileta G, Rodolphe F, Gendrault A, Giraud T, Fournier E, Lopez-Villavicencio M, Gautier A, Lebrun M-H, Chiapello H: Funybase: a fungal phylogenomic database. BMC Bioinforma 2008, 9: 456. 10.1186/1471-2105-9-456
80. Aguileta G, Marthey S, Chiapello H, Lebrun M-H, Rodolphe F, Fournier E, Gendrault-Jacquemard A, Giraud T: Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol 2008, 57: 613-627. 10.1080/10635150802306527
81. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32: 1792-1797. 10.1093/nar/gkh340
82. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 20. Bioinformatics 2007, 23: 2947-2948. 10.1093/bioinformatics/btm404
83. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T: trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25: 1972-1973. 10.1093/bioinformatics/btp348
84. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T: GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 2010,38(Web Server issue):W23-W28.
85. Lanfear R, Calcott B, Ho SYW, Guindon S: Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 2012, 29: 1695-1701. 10.1093/molbev/mss020
86. Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29: 1969-1973. 10.1093/molbev/mss075
87. Lucking R, Huhndorf S, Pfister DH, Plata ER, Lumbsch HT: Fungi evolved right on track. Mycologia 2009, 101: 810-822. 10.3852/09-016
88. Rambaut A, Drummond AJ: Tracer v1.4. 2007.