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

BMC Evolutionary Biology

Timothy I Sawbridge²  John W Forster²  German C Spangenberg²  Kathryn M Guthridge¹  Maia Rabinovich¹  Piyumi N Ekanayake² 

[1] Dairy Futures Cooperative Research Centre, Bundoora, Australia;La Trobe University, Bundoora, Victoria 3086, Australia

关键词: Tub2;    TefA;    PerA;    Whole genome sequencing;    Pasture grass;    Festuca;   

Others  :  858198
DOI  :  10.1186/1471-2148-13-270

 received in 2013-07-17, accepted in 2013-12-06,  发布年份 2013

【 摘 要 】

Background

Tall fescue and meadow fescue are important as temperate pasture grasses, forming mutualistic associations with asexual Neotyphodium endophytes. The most frequently identified endophyte of Continental allohexaploid tall fescue is Neotyphodium coenophialum, while representatives of two other taxa (FaTG-2 and FaTG-3) have been described as colonising decaploid and Mediterranean hexaploid tall fescue, respectively. In addition, a recent study identified two other putatively novel endophyte taxa from Mediterranean hexaploid and decaploid tall fescue accessions, which were designated as uncharacterised Neotyphodium species (UNS) and FaTG-3-like respectively. In contrast, diploid meadow fescue mainly forms associations with the endophyte taxon Neotyphodium uncinatum, although a second endophyte taxon, termed N. siegelii, has also been described.

Results

Multiple copies of the translation elongation factor 1-a (tefA) and β-tubulin (tub2) ‘house-keeping’ genes, as well as the endophyte-specific perA gene, were identified for each fescue-derived endophyte taxon from whole genome sequence data. The assembled gene sequences were used to reconstruct evolutionary relationships between the heteroploid fescue-derived endophytes and putative ancestral sub-genomes derived from known sexual Epichloë species. In addition to the nuclear genome-derived genes, the complete mitochondrial genome (mt genome) sequence was obtained for each of the sequenced endophyte, and phylogenetic relationships between the mt genome protein coding gene complements were also reconstructed.

Conclusions

Complex and highly reticulated evolutionary relationships between Epichloë-Neotyphodium endophytes have been predicted on the basis of multiple nuclear genes and entire mitochondrial protein-coding gene complements, derived from independent assembly of whole genome sequence reads. The results are consistent with previous studies while also providing novel phylogenetic insights, particularly through inclusion of data from the endophyte lineage-specific gene, as well as affording evidence for the origin of cytoplasmic genomes. In particular, the results obtained from the present study imply the possible occurrence of at least two distinct E. typhina progenitors for heteropoid taxa, as well the ancestral contribution of an endophyte species distinct from (although related to) contemporary E. baconii to the extant hybrid species. Furthermore, the present study confirmed the distinct taxonomic status of the newly identified fescue endophyte taxa, FaTG-3-like and UNS, which are consequently proposed to be renamed FaTG4 and FaTG5, respectively.

【 授权许可】

   
2013 Ekanayake et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE: Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 1989, 81:83-90.
• [2]Malinowski DP, Belesky DP: Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 2000, 40:923-940.
• [3]Schardl CL, Young CA, Faulkner JR, Florea S, Pan J: Chemotypic diversity of epichloae, fungal symbionts of grasses. fungal ecology 2012, 5:331-344.
• [4]Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC: Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 1990, 16(12):3301-3315.
• [5]Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP: Loline alkaloids: currencies of mutualism. Phytochemistry 2007, 68:980-996.
• [6]Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B: A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 2005, 57(4):1036-1050.
• [7]Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R: Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. J Chem Soc Chem Commun 1984, 9:614-616.
• [8]Porter JK: Analysis of endophyte toxins - Fescue and other grasses toxic to livestock. J Anim Sci 1995, 73(3):871-880.
• [9]Ekanayake PN, Hand ML, Spangenberg GC, Forster JW, Guthridge KM: Genetic diversity and host specificity of fungal endophyte taxa in fescue pasture grasses. Crop Sci 2012, 52:2243-2252.
• [10]Hand ML, Cogan NOI, Forster JW: Molecular characterisation and interpretation of genetic diversity within globally distributed germplasm collections of tall fescue (Festuca arundinacea Schreb.) and meadow fescue (F. pratensis Huds.). Theor Appl Genet 2012, 124:1127-1137.
• [11]Hand M, Cogan N, Stewart A, Forster J: Evolutionary history of tall fescue morphotypes inferred from molecular phylogenetics of the Lolium-Festuca species complex. BMC Evol Biol 2010, 10(1):303. BioMed Central Full Text
• [12]Glenn AE, Bacon CW, Price R, Hanlin RT: Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 1996, 88(3):369-383.
• [13]Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA: Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial ryegrass (Lolium perenne). Mycol Res 1993, 97(9):1083-1092.
• [14]Schardl C, Young C, Pan J, Florea S, Takach J, Panaccione D, Farman M, Webb J, Jaromczyk J, Charlton N, et al.: Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins 2013, 5(6):1064-1088.
• [15]Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL: Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia 2001, 53(1):44-73.
• [16]Moon CD, Scott B, Schardl CL, Christensen MJ: The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 2000, 92(6):1103-1118.
• [17]Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL: Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 2004, 13:1455-1467.
• [18]Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GCM, Siegel MR, Schardl CL: Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci USA 1994, 91(7):2542-2546.
• [19]van Zijll de Jong E, Guthridge KM, Spangenberg GC, Forster JW: Sequence analysis of SSR-flanking regions identifies genome affinities between pasture grass fungal endophyte taxa. Int J Evol Biol 2011. Article ID 921312, 11 pages, doi:10.4061/2011/921312
• [20]Gentile A, Rossi MS, Cabral D, KC D, Schardl CL: Origin, divergence, and phylogeny of Epichloë endophytes of native Argentine grasses. Mol Phylogenet Evol 2005, 35:196-208.
• [21]Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL: Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Ann Mo Bot Gard 2001, 88(1):14-34.
• [22]Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, et al.: Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the clavicipitaceae reveals dynamics of alkaloid Loci. PLoS Genet 2013, 9(2):28.
• [23]Takach JE, Mittal S, Swoboda GA, Bright SK, Trammell MA, Hopkins AA, Young CA: Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl Environ Microbiol 2012, 78:5501-5510.
• [24]Griffiths AJF: Mitochondrial inheritance in filamentous fungi. J Genet 1996, 75:403-414.
• [25]Gray MW, Burger G, Lang BF: Mitochondrial evolution. Science 1999, 283(5407):1476-1481.
• [26]Gray MW: Mitochondrial evolution. Cold Spring Harb Perspect Biol 2012, 4:9.
• [27]Burger G, Gray MW, Franz Lang B: Mitochondrial genomes: anything goes. Trends Genet 2003, 19(12):709-716.
• [28]Möller EM, Bahnweg G, Sandermann H, Geiger HH: A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies and infected plant tissue. Nucleic Acids Res 1992, 20(22):6115-6116.
• [29]Zerbino DR, Birney E: Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18(5):821-829.
• [30]Altschul S, Gish W, Miller W, Myers E, Lipman D: Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
• [31]Manolo G, Stéphane G, Olivier G: SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27(2):221-224.
• [32]Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, De Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al.: ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 2012, 40:W597-W603.
• [33]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al.: ClustalW and ClustalX version 2. Bioinformatics 2007, 23(21):2947-2948.
• [34]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [35]Bryant D, Moulton V: NeighborNet: an agglomerative algorithm for the construction of phylogenetic networks. Mol Biol Evol 2004, 21:255-265.
• [36]Huson D, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23:254-267.
• [37]Rabinovich M: Genome structure and diversity in the perennial ryegrass (Lolium perenne l.) fungal endophyte Neotyphodium lolii. Bundoora: La trobe University; 2011.
• [38]Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 2009, 25:1754-1760.
• [39]Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, Marshall D: Tablet - next generation sequence assembly visualization. Bioinformatics 2010, 26(3):401-402.
• [40]Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED, Sidow A, Batzoglou S: NISC Comparative Sequencing Program. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 2003, 13(4):721-731.
• [41]Frazer KA, Pachter L, Poliakov A, Rubin EM, I. D: VISTA: computational tools for comparative genomics. Nucleic Acids Res 2004, 1(32):W273-279.
• [42]Moon CD, Miles CO, Jarlfors U, Schardl CL: The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere. Mycologia 2002, 94(4):694-711.
• [43]Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R: A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Syst Biol 2008, 57(3):483-498.
• [44]Chung KR, Leuchtmann A, Schardl CL: Inheritance of mitochondrial DNA and plasmids in the ascomycetous fungus, Epichloë typhina. Genetics 1996, 142(1):259-265.
• [45]Kuldau GA, Tsai HF, Schardl CL: Genome sizes of Epichloë species and anamorphic hybrids. Mycologia 1999, 91(5):776-782.
• [46]Schardl CL, Leuchtmann A, Tsai HF, Collett MA, Watt DM, Scott DB: Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics 1994, 136(4):1307-1317.
• [47]Fleetwood DJ, Khan AK, Johnson RD, Young CA, Mittal S, Wrenn RE, Hesse U, Foster SJ, Schardl CL, B. S: Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses. Genome Biol Evol 2011, 3:1253-1264.