A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi

Genome Biology

Volumn 12, Issue 5, 2011, Pages

  Hane, James K ^a,b   Rouxel, Thierry ^c   Howlett, Barbara J ^d   Kema, Gert H J ^e   Goodwin, Stephen B ^f   Oliver, Richard P ^g  

^a CSIRO   (Australia)

^b MURDOCH UNIVERSITY   (Australia)

^c INRA Institut National de la Recherche Agronomique   (France)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f PURDUE UNIVERSITY   (United States)

^g CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASCOMYCETES; CHROMOSOME ANALYSIS; CHROMOSOME INVERSION; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DOTHIDEOMYCETES; EUKARYOTE EVOLUTION; EVOLUTIONARY HOMOLOGY; FUNGAL GENOME; GENETIC CONSERVATION; MEIOSIS; NONHUMAN; SPECIES COMPARISON; SYNTENY; ALGORITHM; CHEMISTRY; CHROMOSOME; CHROMOSOME MAP; GENETIC DATABASE; GENETICS; GENOMICS; METHODOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPECIES DIFFERENCE;

ASCOMYCOTA; EUKARYOTA; FUNGI;

ALGORITHMS; ASCOMYCOTA; CHROMOSOME INVERSION; CHROMOSOME MAPPING; CHROMOSOMES; CONSERVED SEQUENCE; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENOME, FUNGAL; GENOMICS; MEIOSIS; PHYLOGENY; SPECIES SPECIFICITY; SYNTENY;

EID: 79956280303     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-5-r45     Document Type: Article

References (55)

1. Schoch CL, Sung GH, Lopez-Giraldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh SO, Blackwell M, et al. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 2009, 58:224-239. 10.1093/sysbio/syp020, 20525580.
2. Sims GE, Jun SR, Wu GA, Kim SH. Alignment-free genome comparison with feature frequency profiles (FFP) and optimal resolutions. Proc Natl Acad Sci USA 2009, 106:2677-2682. 10.1073/pnas.0813249106, 2634796, 19188606.
3. McLysaght A, Enright AJ, Skrabanek L, Wolfe KH. Estimation of synteny conservation and genome compaction between pufferfish (Fugu) and human. Yeast 2000, 17:22-36. 10.1002/(SICI)1097-0061(200004)17:1<22::AID-YEA5>3.0.CO;2-S, 2447035, 10797599.
4. Pennacchio LA. Insights from human/mouse genome comparisons. Mamm Genome 2003, 14:429-436. 10.1007/s00335-002-4001-1, 12925891.
5. Kohn M, Kehrer-Sawatzki H, Vogel W, Graves JA, Hameister H. Wide genome comparisons reveal the origins of the human X chromosome. Trends Genet 2004, 20:598-603. 10.1016/j.tig.2004.09.008, 15522454.
6. Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, Gouzy J, Wang X, Mudge J, Vasdewani J, Schiex T, Spannagl M, Monaghan E, Nicholson C, Humphray SJ, Schoof H, Mayer KF, Rogers J, Quetier F, Oldroyd GE, Debelle F, Cook DR, Retzel EF, Roe BA, Town CD, Tabata S, Van de Peer Y, Young ND. Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci USA 2006, 103:14959-14964. 10.1073/pnas.0603228103, 1578499, 17003129.
7. Phan HT, Ellwood SR, Hane JK, Ford R, Materne M, Oliver RP. Extensive macrosynteny between Medicago truncatula and Lens culinaris ssp. culinaris. Theor Appl Genet 2007, 114:549-558. 10.1007/s00122-006-0455-3, 17119911.
8. Shultz JL, Ray JD, Lightfoot DA. A sequence based synteny map between soybean and Arabidopsis thaliana. BMC Genomics 2007, 8:8. 10.1186/1471-2164-8-8, 1780048, 17210083.
9. Parkin AP, Lydiate DJ, Trick M. Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 2002, 45:356-366. 10.1139/g01-160, 11962633.
10. Ma B. Synteny between Brachypodium distachyon and Hordeum vulgare as revealed by FISH. Chromosome Res 2010, 18:841-850. 10.1007/s10577-010-9166-3, 21104310.
11. Zhang Y, Schoch CL, Fournier J, Crous PW, de Gruyter J, Woudenberg JH, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD. Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 2009, 64:85-102S5. 10.3114/sim.2009.64.04, 2816967, 20169024.
12. Marande W, López-García P, Moreira D. Eukaryotic diversity and phylogeny using small- and large-subunit ribosomal RNA genes from environmental samples. Environ Microbiol 2009, 11:3179-3188. 10.1111/j.1462-2920.2009.02023.x, 19678831.
13. Wang H, Guo S, Huang M, Thorsten LH, Wei J. Ascomycota has a faster evolutionary rate and higher species diversity than Basidiomycota. Sci China 2010, 53:1163-1169.
14. Oliver RP, Solomon PS. Recent fungal diseases of crop plants: is lateral gene transfer a common theme?. Mol Plant Microbe Interact 2008, 21:287-293. 10.1094/MPMI-21-3-0287, 18257678.
15. Marcet-Houben M, Gabaldon T. Acquisition of prokaryotic genes by fungal genomes. Trends Genet 2010, 26:5-8. 10.1016/j.tig.2009.11.007, 19969385.
16. 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, 16832356.
17. Chibana H, Oka N, Nakayama H, Aoyama T, Magee BB, Magee PT, Mikami Y. Sequence finishing and gene mapping for Candida albicans chromosome 7 and syntenic analysis against the Saccharomyces cerevisiae genome. Genetics 2005, 170:1525-1537. 10.1534/genetics.104.034652, 1449773, 15937140.
18. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, et al. Lessons from the genome sequence of Neurospora crassa: Tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 2004, 68:1-108. 10.1128/MMBR.68.1.1-108.2004, 362109, 15007097.
19. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986. 10.1038/nature03449, 15846337.
20. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Segurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Dequard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarre B, et al. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 2008, 9:R77. 10.1186/gb-2008-9-5-r77, 2441463, 18460219.
21. Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SF, McDonald BA, Oliver RP. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 2007, 19:3347-3368. 10.1105/tpc.107.052829, 2174895, 18024570.
22. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, Garcia JL, Garcia MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, et al. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438:1151-1156. 10.1038/nature04332, 16372009.
23. Machida M, Terabayashi Y, Sano M, Yamane N, Tamano K, Payne GA, Yu J, Cleveland TE, Nierman WC. Genomics of industrial Aspergilli and comparison with toxigenic relatives. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2008, 25:1147-1151.
24. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, et al. Genome sequencing and analysis of Aspergillus oryzae. Nature 2005, 438:1157-1161. 10.1038/nature04300, 16372010.
25. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d'Enfert C, Geysens S, Goosen C, Groot GS, et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 2007, 25:221-231. 10.1038/nbt1282, 17259976.
26. Maizel JV, Lenk RP. Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc Natl Acad Sci USA 1981, 78:7665-7669. 10.1073/pnas.78.12.7665, 349330, 6801656.
27. Solomon PS, Lowe RGT, Tan KC, Waters ODC, Oliver RP. Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Mol Plant Pathol 2006, 7:147-156. 10.1111/j.1364-3703.2006.00326.x, 20507435.
28. Schoch CL, Crous PW, Groenewald JZ, Boehm EW, Burgess TI, de Gruyter J, de Hoog GS, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya T, Huhndorf SM, Hyde KD, Jones EB, Kohlmeyer J, Kruys A, Li YM, Lucking R, Lumbsch HT, Marvanova L, Mbatchou JS, McVay AH, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, et al. A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 2009, 64:1-15S10. 10.3114/sim.2009.64.01, 2816964, 20169021.
29. Cooley RN, Caten CE. Variation in electrophoretic karyotype between strains of Septoria nodorum. Mol Gen Genet 1991, 228:17-23.
30. Bringans S, Hane JK, Casey T, Tan KC, Lipscombe R, Solomon PS, Oliver RP. Deep proteogenomics; high throughput gene validation by multidimensional liquid chromatography and mass spectrometry of proteins from the fungal wheat pathogen Stagonospora nodorum. BMC Bioinformatics 2009, 10:301. 10.1186/1471-2105-10-301, 2753851, 19772613.
31. Casey T, Solomon PS, Bringans S, Tan KC, Oliver RP, Lipscombe R. Quantitative proteomic analysis of G-protein signalling in Stagonospora nodorum using isobaric tags for relative and absolute quantification. Proteomics 2010, 10:38-47. 10.1002/pmic.200900474, 19882661.
32. Tan K-C, Heazlewood JL, Millar AH, Oliver RP, Solomon PS. Proteomic identification of extracellular proteins regulated by the Gna1 Gα subunit in Stagonospora nodorum. Mycol Res 2009, 113:523-531. 10.1016/j.mycres.2009.01.004, 19284980.
33. Oliver RP, Solomon PS. New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 2010, 13:415-419. 10.1016/j.pbi.2010.05.003, 20684067.
34. Liu Z, Faris JD, Oliver RP, Tan KC, Solomon PS, McDonald MC, McDonald BA, Nunez A, Lu S, Rasmussen JB, Friesen TL. SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Path 2009, 5:e1000581.
35. Friesen TL, Faris JD, Solomon PS, Oliver RP. Host-specific toxins: Effectors of necrotrophic pathogenicity. Cell Microbiol 2008, 10:1421-1428. 10.1111/j.1462-5822.2008.01153.x, 18384660.
36. Friesen TL, Zhang Z, Solomon PS, Oliver RP, Faris JD. Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiol 2008, 146:682-693. 2245837, 18065563.
37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol 2004, 5:R12. 10.1186/gb-2004-5-2-r12, 395750, 14759262.
38. Rouxel T, Grandaubert J, Hane J, Hoede C, van de Wouw A, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen A, Ciuffetti L, Dimaghani A, Duret L, Fudal I, Goodwin S, Gout L, Glaser N, Kema G, Lapalu N, Lawrence C, May K, Meyer M, Ollivier B, Poulain J, Turgeon G, Tyler BM, Vincent D, Weissenbach J, Amselem J, et al. The compartmentalized genome of Leptosphaeria maculans: diversification of effectors within genomic regions affected by Repeat Induced Point mutations. Nat Commun 2011, 2:art.202.
39. Goodwin SB, Ben M'Barek S, Dhillon B, Wittenberg A, Crane CF, Van der Lee TAJ, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, Brokstein P, Canto-Canche B, Churchill A, Conde-Ferràez L, Cools H, Coutinho PM, Csukai M, Dehal P, Donzelli B, Foster AJ, Hammond-Kosack K, Hane J, Henrissat B, Kilian A, Koopmann E, Kourmpetis Y, Kuo A, et al. Finished genome of Mycosphaerella graminicola reveals stealth pathogenesis and dispensome structure. PLoS Genetics -D-10-00112R2 2011,
40. Passarge E, Horsthemke B, Farber RA. Incorrect use of the term synteny. Nat Genet 1999, 23:387.
41. Broad Institute. , http://www.broadinstitute.org/
42. DOE Joint Genome Institute. , http://www.jgi.doe.gov/
43. S. sclerotiorum Sequencing Project. , http://www.broadinstitute.org/annotation/genome/sclerotinia_sclerotiorum/Info.html
44. Giles NH, Geever RF, Asch DK, Avalos J, Case ME. Organization and regulation of the qa (quinic acid) genes in Neurospora crassa and other fungi. J Hered 1991, 82:1-7.
45. Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu K, Benito-Gutiérrez T, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, De Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071. 10.1038/nature06967, 18563158.
46. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury JM, Ballario P, Bolchi A, Brenna A, Brun A, Buee M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038. 10.1038/nature08867, 20348908.
47. Yun SH, Arie T, Kaneko I, Yoder OC, Turgeon BG. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 2000, 31:7-20. 10.1006/fgbi.2000.1226, 11118131.
48. Fisher MC, Hanage WP, De Hoog S, Johnson E, Smith MD, White NJ, Vanittanakom N. Low effective dispersal of asexual genotypes in heterogeneous landscapes by the endemic pathogen penicillium marneffei. PLoS Path 2005, 1:0159-0165.
49. Wittenberg AH, van der Lee TA, Ben M'barek S, Ware SB, Goodwin SB, Kilian A, Visser RG, Kema GH, Schouten HJ. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 2009, 4:e5863. 10.1371/journal.pone.0005863, 2689623, 19516898.
50. 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, et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373. 10.1038/nature08850, 3048781, 20237561.
51. Clutterbuck JA. Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 2011, 48:306-326. 10.1016/j.fgb.2010.09.002, 20854921.
52. Akagi Y, Akamatsu H, Otani H, Kodama M. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 2009, 8:1732-1738. 10.1128/EC.00135-09, 2772402, 19749175.
53. Roca M, Read N, Wheals A. Conidial anastomosis tubes in filamentous fungi. FEMS Micro Letts 2005, 249:191-198.
54. Liu Y, Leigh JW, Brinkmann H, Cushion MT, Rodriguez-Ezpeleta N, Philippe H, Lang BF. Phylogenomic analyses support the monophyly of Taphrinomycotina, including Schizosaccharomyces fission yeasts. Mol Biol Evol 2009, 26:27-34.
55. Shertz CA, Bastidas RJ, Li W, Heitman J, Cardenas ME. Conservation, duplication, and loss of the Tor signaling pathway in the fungal kingdom. BMC Genomics 2010, 11:510. 10.1186/1471-2164-11-510, 2997006, 20863387.