Phylogenomics of fescue grass-derived fungal endophytes based on selected nuclear genes and the mitochondrial gene complement

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Ekanayake, Piyumi N ^a,b,c   Rabinovich, Maia ^a,b   Guthridge, Kathryn M ^a,b   Spangenberg, German C ^a,b,c   Forster, John W ^a,b,c   Sawbridge, Timothy I ^a,b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b Dairy Futures Cooperative Research Centre   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Festuca; Pasture grass; PerA; TefA; Tub2; Whole genome sequencing

Indexed keywords

ANCESTRY; ENDOPHYTE; FUNGUS; GENE EXPRESSION; GENOME; GRASS; MITOCHONDRION; MUTUALISM; NEW SPECIES; PHYLOGENETICS; PROTEIN; TAXONOMY;

EPICHLOE; EPICHLOE BACONII; EPICHLOE TYPHINA; FESTUCA; FESTUCA ARUNDINACEA; FESTUCA PRATENSIS; NEOTYPHODIUM; NEOTYPHODIUM COENOPHIALUM; NEOTYPHODIUM SIEGELII; NEOTYPHODIUM UNCINATUM; PERA; POACEAE;

TUBULIN;

ARTICLE; CELL NUCLEUS; CLASSIFICATION; ENDOPHYTE; EPICHLOE; EVOLUTION; FESCUE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MITOCHONDRIAL GENE; NEOTYPHODIUM; PHYLOGENY; PHYSIOLOGY;

BIOLOGICAL EVOLUTION; CELL NUCLEUS; ENDOPHYTES; EPICHLOE; FESTUCA; GENES, MITOCHONDRIAL; NEOTYPHODIUM; PHYLOGENY; TUBULIN;

EID: 84889961736     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-270     Document Type: Article

References (47)

1. Effect of the tall fescue endophyte on plant response to environmental stress. Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE, Agron J 1989 81 83 90 10.2134/agronj1989.00021962008100010015x
2. Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Malinowski DP, Belesky DP, Crop Sci 2000 40 923 940 10.2135/cropsci2000.404923x
3. Chemotypic diversity of epichloae, fungal symbionts of grasses. Schardl CL, Young CA, Faulkner JR, Florea S, Pan J, fungal ecology 2012 5 331 344 10.1016/j.funeco.2011.04.005
4. Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC, J Chem Ecol 1990 16 12 3301 3315 10.1007/BF00982100 24263431
5. Loline alkaloids: currencies of mutualism. Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP, Phytochemistry 2007 68 980 996 10.1016/j.phytochem.2007.01.010 17346759
6. A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B, Mol Microbiol 2005 57 4 1036 1050 10.1111/j.1365-2958.2005.04747.x 16091042
7. Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R, J Chem Soc Chem Commun 1984 9 614 616
8. Analysis of endophyte toxins-Fescue and other grasses toxic to livestock. Porter JK, J Anim Sci 1995 73 3 871 880 7608022
9. Genetic diversity and host specificity of fungal endophyte taxa in fescue pasture grasses. Ekanayake PN, Hand ML, Spangenberg GC, Forster JW, Guthridge KM, Crop Sci 2012 52 2243 2252 10.2135/cropsci2011.12.0664
10. Molecular characterisation and interpretation of genetic diversity within globally distributed germplasm collections of tall fescue (Festuca arundinacea Schreb.) and meadow fescue (F. pratensis Huds.). Hand ML, Cogan NOI, Forster JW, Theor Appl Genet 2012 124 1127 1137 10.1007/s00122-011-1774-6 22222441
11. Evolutionary history of tall fescue morphotypes inferred from molecular phylogenetics of the Lolium-Festuca species complex. Hand M, Cogan N, Stewart A, Forster J, BMC Evol Biol 2010 10 1 303 10.1186/1471-2148-10-303 20937141
12. Molecular phylogeny of Acremonium and its taxonomic implications. Glenn AE, Bacon CW, Price R, Hanlin RT, Mycologia 1996 88 3 369 383 10.2307/3760878
13. Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial ryegrass (Lolium perenne). Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA, Mycol Res 1993 97 9 1083 1092 10.1016/S0953-7562(09)80509-1
14. Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Schardl C, Young C, Pan J, Florea S, Takach J, Panaccione D, Farman M, Webb J, Jaromczyk J, Charlton N, et al. Toxins 2013 5 6 1064 1088 10.3390/toxins5061064 23744053
15. Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL, Sydowia 2001 53 1 44 73
16. The evolutionary origins of Epichloë endophytes from annual ryegrasses. Moon CD, Scott B, Schardl CL, Christensen MJ, Mycologia 2000 92 6 1103 1118 10.2307/3761478
17. Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL, Mol Ecol 2004 13 1455 1467 10.1111/j.1365-294X.2004.02138.x 15140090
18. Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GCM, Siegel MR, Schardl CL, Proc Natl Acad Sci USA 1994 91 7 2542 2546 10.1073/pnas.91.7.2542 8172623
19. Sequence analysis of SSR-flanking regions identifies genome affinities between pasture grass fungal endophyte taxa. van Zijll de Jong E, Guthridge KM, Spangenberg GC, Forster JW, Int J Evol Biol 2011 Article ID 921312, 11 pages, doi:10.4061/2011/921312
20. Origin, divergence, and phylogeny of Epichloë endophytes of native Argentine grasses. Gentile A, Rossi MS, Cabral D, KC D, Schardl CL, Mol Phylogenet Evol 2005 35 196 208 10.1016/j.ympev.2005.01.008 15737591
21. Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL, Ann Mo Bot Gard 2001 88 1 14 34 10.2307/2666129
22. Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid Loci. Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, et al. PLoS Genet 2013 9 2 28
23. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Takach JE, Mittal S, Swoboda GA, Bright SK, Trammell MA, Hopkins AA, Young CA, Appl Environ Microbiol 2012 78 5501 5510 10.1128/AEM.01084-12 22660705
24. Mitochondrial inheritance in filamentous fungi. Griffiths AJF, J Genet 1996 75 403 414 10.1007/BF02966318
25. Mitochondrial evolution. Gray MW, Burger G, Lang BF, Science 1999 283 5407 1476 1481 10.1126/science.283.5407.1476 10066161
26. Mitochondrial evolution. Gray MW, Cold Spring Harb Perspect Biol 2012 4 9
27. Mitochondrial genomes: anything goes. Burger G, Gray MW, Franz Lang B, Trends Genet 2003 19 12 709 716 10.1016/j.tig.2003.10.012 14642752
28. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies and infected plant tissue. Möller EM, Bahnweg G, Sandermann H, Geiger HH, Nucleic Acids Res 1992 20 22 6115 6116 10.1093/nar/20.22.6115 1461751
29. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Zerbino DR, Birney E, Genome Res 2008 18 5 821 829 10.1101/gr.074492.107 18349386
30. Basic local alignment search tool. Altschul S, Gish W, Miller W, Myers E, Lipman D, J Mol Biol 1990 215 3 403 410 2231712
31. SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Manolo G, Stéphane G, Olivier G, Mol Biol Evol 2010 27 2 221 224 10.1093/molbev/msp259 19854763
32. ExPASy: SIB bioinformatics resource portal. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, De Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al. Nucleic Acids Res 2012 40 597 W603 10.1093/nar/gks400 22661580
33. ClustalW and ClustalX version 2. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Bioinformatics 2007 23 21 2947 2948 10.1093/bioinformatics/btm404 17846036
34. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739 10.1093/molbev/msr121 21546353
35. NeighborNet: an agglomerative algorithm for the construction of phylogenetic networks. Bryant D, Moulton V, Mol Biol Evol 2004 21 255 265 14660700
36. Application of phylogenetic networks in evolutionary studies. Huson D, Bryant D, Mol Biol Evol 2006 23 254 267 16221896
37. Rabinovich M, Genome structure and diversity in the perennial ryegrass (Lolium perenne l.) fungal endophyte Neotyphodium lolii Bundoora: La trobe University 2011
38. Fast and accurate short read alignment with Burrows-Wheeler Transform. Li H, Durbin R, Bioinformatics 2009 25 1754 1760 10.1093/bioinformatics/btp324 19451168
39. Tablet-next generation sequence assembly visualization. Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, Marshall D, Bioinformatics 2010 26 3 401 402 10.1093/bioinformatics/btp666 19965881
40. NISC Comparative Sequencing Program. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED, Sidow A, Batzoglou S, Genome Res 2003 13 4 721 731 10.1101/gr.926603 12654723
41. VISTA: computational tools for comparative genomics. Frazer KA, Pachter L, Poliakov A, Rubin EM, I. D, Nucleic Acids Res 2004 1 32 273 279
42. The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere. Moon CD, Miles CO, Jarlfors U, Schardl CL, Mycologia 2002 94 4 694 711 10.2307/3761720 21156542
43. A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R, Syst Biol 2008 57 3 483 498 10.1080/10635150802172184 18570040
44. Inheritance of mitochondrial DNA and plasmids in the ascomycetous fungus, Epichloë typhina. Chung KR, Leuchtmann A, Schardl CL, Genetics 1996 142 1 259 265 8770603
45. Genome sizes of Epichloë species and anamorphic hybrids. Kuldau GA, Tsai HF, Schardl CL, Mycologia 1999 91 5 776 782 10.2307/3761531
46. Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Schardl CL, Leuchtmann A, Tsai HF, Collett MA, Watt DM, Scott DB, Genetics 1994 136 4 1307 1317 8013907
47. Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses. Fleetwood DJ, Khan AK, Johnson RD, Young CA, Mittal S, Wrenn RE, Hesse U, Foster SJ, Schardl CL, B. S, Genome Biol Evol 2011 3 1253 1264 10.1093/gbe/evr098 21948396