Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Schardl, Christopher L ^a   Young, Carolyn A ^b   Hesse, Uljana ^a   Amyotte, Stefan G ^a   Andreeva, Kalina ^a   Calie, Patrick J ^c   Fleetwood, Damien J ^d   Haws, David C ^a   Moore, Neil ^e   Oeser, Birgitt ^f   Panaccione, Daniel G ^g   Schweri, Kathryn K ^a   Voisey, Christine R ^h   Farman, Mark L ^a   Jaromczyk, Jerzy W ^e   Roe, Bruce A ⁱ   O'Sullivan, Donal M ^j   Scott, Barry ^k   Tudzynski, Paul ^f   An, Zhiqiang ^l   Arnaoudova, Elissaveta G ^e   Bullock, Charles T ^e   Charlton, Nikki D ^b   Chen, Li ^a   Cox, Murray ^k   Dinkins, Randy D ^m   Florea, Simona ^a   Glenn, Anthony E ⁿ   Gordon, Anna ^j   Güldener, Ulrich ^o   Harris, Daniel R ^e   Hollin, Walter ^a   Jaromczyk, Jolanta ^a   Johnson, Richard D ^h   Khan, Anar K ^p   Leistner, Eckhard ^q   Leuchtmann, Adrian ^r   Li, Chunjie ^s   Liu, JinGe ^a   Liu, Jinze ^e   Liu, Miao ^a   Mace, Wade ^h   Machado, Caroline ^a   Nagabhyru, Padmaja ^a   Pan, Juan ^a   Schmid, Jan ^k   Sugawara, Koya ^t   Steiner, Ulrike ^q   Takach, Johanna E ^b   Tanaka, Eiji ^u   Webb, Jennifer S ^a   Wilson, Ella V ^a   Wiseman, Jennifer L ^a   Yoshida, Ruriko ^a   Zeng, Zheng ^e   more..

^a UNIVERSITY OF KENTUCKY   (United States)

^b PLANT BIOLOGY DIVISION   (United States)

^c EASTERN KENTUCKY UNIVERSITY   (United States)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e UNIVERSITY OF KENTUCKY   (United States)

^f UNIVERSITY OF MÜNSTER   (Germany)

^g WEST VIRGINIA UNIVERSITY   (United States)

^h AGRESEARCH GRASSLANDS   (New Zealand)

ⁱ UNIVERSITY OF OKLAHOMA   (United States)

^j NATIONAL INSTITUTE OF AGRICULTURAL BOTANY   (United Kingdom)

^k MASSEY UNIVERSITY   (New Zealand)

^l UNIVERSITY OF TEXAS   (United States)

^m U S DEPARTMENT OF AGRICULTURE   (United States)

ⁿ RUSSELL RESEARCH CENTER   (United States)

^o INSTITUTE OF EPIDEMIOLOGY   (Germany)

^p INVERMAY AGRICULTURAL CENTRE   (New Zealand)

^q UNIVERSITY OF BONN   (Germany)

^r ETH ZURICH   (Switzerland)

^s LANZHOU UNIVERSITY   (China)

^t FOOD RESEARCH INSTITUTE   (Japan)

^u ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID;

ACICULOSPORIUM TAKE; ARTICLE; CHEMICAL ENGINEERING; CLAVICEPS; CLAVICIPITACEAE; CONTROLLED STUDY; EPICHLOE; FUNGUS; GENE CLUSTER; GENE DUPLICATION; GENE FUNCTION; GENE LOCUS; GENE LOSS; GENE SEQUENCE; GENE STRUCTURE; GENETIC CONSERVATION; GENOME; GENOME ANALYSIS; NONHUMAN; PERIGLANDULA IPOMOEAE; SYMBIOSIS;

ALKALOIDS; CLAVICEPS; EPICHLOE; ERGOT ALKALOIDS; GENE EXPRESSION REGULATION, FUNGAL; HYPOCREALES; NEOTYPHODIUM; POACEAE; SELECTION, GENETIC; SYMBIOSIS;

EID: 84874772540     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003323     Document Type: Article

References (121)

1. Wink M (2000) Interference of alkaloids with neuroreceptors and ion channels. In: Atta-ur-Rahman, editor. Bioactive Natural Products (Part B): Elsevier. pp. 3-122.
2. Pažoutová S, Olšovská J, Linka M, Kolínská R, Flieger M, (2000) Chemoraces and habitat specialization of Claviceps purpurea populations. Appl Environ Microbiol 66: 5419-5425.
3. Uhlig S, Botha CJ, Vrålstad T, Rolén E, Miles CO, (2009) Indole-diterpenes and ergot alkaloids in Cynodon dactylon (Bermuda grass) infected with Claviceps cynodontis from an outbreak of tremors in cattle. J Agric Food Chem 57: 11112-11119.
4. Schardl CL, Leuchtmann A, Spiering MJ, (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55: 315-340.
5. Iannone LJ, Novas MaV, Young CA, De Battista JP, Schardl CL, (2012) Endophytes of native grasses from South America: Biodiversity and ecology. Fungal Ecology 5: 357-363.
6. Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JF, (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16: 1701-1711.
7. Schardl CL, Panaccione DG, Tudzynski P, (2006) Ergot alkaloids-biology and molecular biology. Alkaloids Chem Biol 63: 45-86.
8. Clay K, Schardl C, (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160: S99-S127.
9. Steiner U, Leibner S, Schardl CL, Leuchtmann A, Leistner E, (2011) Periglandula, a new fungal genus within the Clavicipitaceae and its association with Convolvulaceae. Mycologia 103: 1133-1145.
10. Rudgers JA, Koslow JM, Clay K, (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett 7: 42-51.
11. Malinowski DP, Belesky DP, (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: Mechanisms of drought and mineral stress tolerance. Crop Sci 40: 923-940.
12. Tudzynski P, Correia T, Keller U, (2001) Biotechnology and genetics of ergot alkaloids. Appl Microbiol Biotechnol 57: 593-605.
13. Wiesemuller W, (2005) Present and historical significance of ergot. Ernährungs Umschau 52: 147-148.
14. Giger RKA, Engel G, (2006) Albert Hofmann's pioneering work on ergot alkaloids and its impact on the search of novel drugs at Sandoz, a predecessor company of Novartis. CHIMIA International Journal for Chemistry 60: 83-87.
15. Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP, (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68: 980-996.
16. Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B, (2005) 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 57: 1036-1050.
17. Bacetty AA, Snook ME, Glenn AE, Noe JP, Hill N, et al. (2009) Toxicity of endophyte-infected tall fescue alkaloids and grass metabolites on Pratylenchus scribneri. Phytopathology 99: 1336-1345.
18. Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, et al. (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J 94: 567-574.
19. Lyons PC, Plattner RD, Bacon CW, (1986) Occurrence of peptide and clavine ergot alkaloids in tall fescue grass. Science 232: 487-489.
20. Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R, (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. J Chem Soc Chem Commun 1984: 614-616.
21. Markert A, Steffan N, Ploss K, Hellwig S, Steiner U, et al. (2008) Biosynthesis and accumulation of ergoline alkaloids in a mutualistic association between Ipomoea asarifolia (Convolvulaceae) and a clavicipitalean fungus. Plant Physiol 147: 296-305.
22. Tor-Agbidye J, Blythe LL, Craig AM, (2001) Correlation of endophyte toxins (ergovaline and lolitrem B) with clinical disease: fescue foot and perennial ryegrass staggers. Vet Hum Toxicol 43: 140-146.
23. Thompson RW, Fribourg HA, Waller JC, Sanders WL, Reynolds JH, et al. (1993) Combined analysis of tall fescue steer grazing studies in the eastern United States. J Anim Sci 71: 1940-1946.
24. Schardl CL, Young CA, Faulkner JR, Florea S, Pan J, (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol 5: 331-344.
25. Schardl CL, (2010) The epichloae, symbionts of the grass subfamily Poöideae. Ann Mo Bot Gard 97: 646-665.
26. Zhang D-X, Nagabhyru P, Blankenship JD, Schardl CL, (2010) Are loline alkaloid levels regulated in grass endophytes by gene expression or substrate availability? Plant Signal Behav 5: 1419-1422.
27. Leuchtmann A, Schmidt D, Bush LP, (2000) Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. J Chem Ecol 26: 1025-1036.
28. Saari S, Helander M, Lehtonen P, Wallius E, Saikkonen K, (2010) Fungal endophytes reduce regrowth and affect competitiveness of meadow fescue in early succession of pastures. Grass and Forage Science 65: 287-295.
29. Afkhami ME, Rudgers JA, (2009) Endophyte-mediated resistance to herbivores depends on herbivore identity in the wild grass Festuca subverticillata. Environ Entomol 38: 1086-1095.
30. Crosignani PG, (2006) Current treatment issues in female hyperprolactinaemia. Eur J Obstet Gynecol Reprod Biol 125: 152-164.
31. Nichols DE (2001) LSD and its lysergamide cousins. The Heffter Review of Psychedelic Research. Santa Fe, New Mexico: Heffter Research Institute. pp. 80-87.
32. Eadie MJ, (2003) Convulsive ergotism: epidemics of the serotonin syndrome? Lancet Neurol 2: 429-434.
33. Caporael LR, (1976) Ergotism: the Satan loosed in Salem? Science 192: 21-26.
34. Scott P, (2009) Ergot alkaloids: extent of human and animal exposure. World Mycotoxin Journal 2: 141-149.
35. Urga K, Debella A, W'Medihn Y, N A, Bayu A, et al. (2002) Laboratory studies on the outbreak of gangrenous ergotism associated with consumption of contaminated barley in Arsi, Ethiopia. Ethiopian Journal of Health and Development 16: 317-323.
36. Smith MM, Warren VA, Thomas BS, Brochu RM, Ertel EA, et al. (2000) Nodulisporic acid opens insect glutamate-gated chloride channels: identification of a new high affinity modulator. Biochemistry 39: 5543-5554.
37. Knaus HG, McManus OB, Lee SH, Schmalhofer WA, Garcia-Calvo M, et al. (1994) Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry 33: 5819-5828.
38. Young C, McMillan L, Telfer E, Scott B, (2001) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Penicillium paxilli. Mol Microbiol 39: 754-764.
39. Tsai H-F, Wang H, Gebler JC, Poulter CD, Schardl CL, (1995) The Claviceps purpurea gene encoding dimethylallyltryptophan synthase, the committed step for ergot alkaloid biosynthesis. Biochem Biophys Res Commun 216: 119-125.
40. Spiering MJ, Wilkinson HH, Blankenship JD, Schardl CL, (2002) Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum. Fungal Genet Biol 36: 242-254.
41. Lorenz N, Haarmann T, Pažoutová S, Jung M, Tudzynski P, (2009) The ergot alkaloid gene cluster: Functional analyses and evolutionary aspects. Phytochemistry 70: 1822-1832.
42. Spiering MJ, Moon CD, Wilkinson HH, Schardl CL, (2005) Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169: 1403-1414.
43. Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, et al. (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43: 679-693.
44. Sung GH, Sung JM, Hywel Jones NL, Spatafora JW, (2007) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 44: 1204-1223.
45. Tanaka E, Tanaka C, (2008) Phylogenetic study of clavicipitaceous fungi using acetaldehyde dehydrogenase gene sequences. Mycoscience 49: 115-125.
46. Gao Q, Jin K, Ying S-H, Zhang Y, Xiao G, et al. (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7: e1001264 doi:10.1371/journal.pgen.1001264.
47. Pava-Ripoll M, Angelini C, Fang W, Wang S, Posada FJ, et al. (2011) The rhizosphere-competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology 157: 47-55.
48. Fleetwood DJ, Scott B, Lane GA, Tanaka A, Johnson RD, (2007) A complex ergovaline gene cluster in epichloë endophytes of grasses. Appl Environ Microbiol 73: 2571-2579.
49. Steiner U, Leistner E, (2012) Ergoline alkaloids in convolvulaceous host plants originate from epibiotic clavicipitaceous fungi of the genus Periglandula. Fungal Ecol 5: 316-321.
50. Gröger D, Floss HG (1998) Biochemistry of ergot alkaloids - achievements and challenges. In: Cordell GA, editor. Alkaloids Chem Biol. New York: Academic Press. pp. 171-218.
51. Haarmann T, Lorenz N, Tudzynski P, (2008) Use of a nonhomologous end joining deficient strain (Δku70) of the ergot fungus Claviceps purpurea for identification of a nonribosomal peptide synthetase gene involved in ergotamine biosynthesis. Fungal Genet Biol 45: 35-44.
52. Castagnoli N Jr, Corbett K, Chain EB, Thomas R, (1970) Biosynthesis of N-(α-hydroxyethyl) lysergamide, a metabolite of Claviceps paspali Stevens and Hall. Biochem J 117: 451-455.
53. Saikia S, Takemoto D, Tapper BA, Lane GA, Frazer K, et al. (2012) Functional analysis of an indole-diterpene gene cluster for lolitrem B biosynthesis in the grass endosymbiont Epichloë festucae. FEBS Lett (in press).
54. Cole RJ, Dorner JW, Lansden JA, Cox RH, Pape C, et al. (1977) Paspalum staggers: isolation and identification of tremorgenic metabolites from sclerotia of Claviceps paspali. J Agric Food Chem 25: 1197-1201.
55. Li SM, Unsold IA, (2006) Post-genome research on the biosynthesis of ergot alkaloids. Planta Med 72: 1117-1120.
56. Saikia S, Parker EJ, Koulman A, Scott B, (2007) Defining paxilline biosynthesis in Penicillium paxilli: functional characterization of two cytochrome P450 monooxygenases. J Biol Chem 282: 16829-16837.
57. Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, et al. (2010) Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiology 153: 1780-1794.
58. Tusnády GE, Simon I, (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850.
59. Krogh A, Larsson Br, von Heijne G, Sonnhammer ELL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
60. Masami I, Masafumi A, Demelo ML, Toshio S, (2002) Transmembrane topology prediction methods: a re-assessment and improvement by a consensus method using a dataset of experimentally-characterized transmembrane topologies. In Silico Biol 2: 19-33.
61. Saikia S, Parker EJ, Koulman A, Scott B, (2006) Four gene products are required for the fungal synthesis of the indole-diterpene, paspaline. FEBS Lett 580: 1625-1630.
62. Kutil BL, Greenwald C, Liu G, Spiering MJ, Schardl CL, et al. (2007) Comparison of loline alkaloid gene clusters across fungal endophytes: Predicting the co-regulatory sequence motifs and the evolutionary history. Fungal Genet Biol 44: 1002-1010.
63. Gao WM, Khang CH, Park SY, Lee YH, Kang SC, (2002) Evolution and organization of a highly dynamic, subtelomeric helicase gene family in the rice blast fungus Magnaporthe grisea. Genetics 162: 103-112.
64. Cuomo CA, Guldener U, Xu J-R, Trail F, Turgeon BG, et al. (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400-1402.
65. Clutterbuck AJ, (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48: 306-326.
66. Freitag M, Williams RL, Kothe GO, Selker EU, (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci U S A 99: 8802-8807.
67. Fleetwood DJ, Khan AK, Johnson RD, Young CA, Mittal S, et al. (2011) Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses. Genome Biol Evol 3: 1253-1264.
68. Philippi T, Seger J, (1989) Hedging one's evolutionary bets, revisited. Trends Ecol Evol 4: 41-44.
69. Svardal H, Rueffler C, Hermisson J, (2011) Comparing environmental and genetic variance as adaptive response to fluctuating selection. Evolution 65: 2492-2513.
70. Lorenz N, Wilson EV, Machado C, Schardl CL, Tudzynski P, (2007) Comparison of ergot alkaloid biosynthesis gene clusters in Claviceps species indicates loss of late pathway steps in evolution of C. fusiformis. Appl Environ Microbiol 73: 7185-7191.
71. Young C, Bryant M, Christensen M, Tapper B, Bryan G, et al. (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Genet Genomics 274: 13-29.
72. Spiering MJ, Faulkner JR, Zhang D-X, Machado C, Grossman RB, et al. (2008) Role of the LolP cytochrome P450 monooxygenase in loline alkaloid biosynthesis. Fungal Genet Biol 45: 1307-1314.
73. Blaney BJ, Maryam R, Murray S-A, Ryley MJ, (2003) Alkaloids of the sorghum ergot pathogen (Claviceps africana): assay methods for grain and feed and variation between sclerotia/sphacelia. Aust J Agric Res 54: 167-175.
74. Coyle CM, Cheng JZ, O'Connor SE, Panaccione DG, (2010) An old yellow enzyme gene controls the branch point between Aspergillus fumigatus and Claviceps purpurea ergot alkaloid pathways. Appl Environ Microbiol 76: 3898-3903.
75. Haarmann T, Ortel I, Tudzynski P, Keller U, (2006) Identification of the cytochrome P450 monooxygenase that bridges the clavine and ergoline alkaloid pathways. Chembiochem 7: 645-652.
76. Kidwell MG, (2002) Genome evolution- Lateral DNA transfer mechanism and consequences. Science 295: 2219-2220.
77. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, et al. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun 2: 202.
78. Ewald PW, (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503: 295-306.
79. Zhang D-X, Nagabhyru P, Schardl CL, (2009) Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiol 150: 1072-1082.
80. Mey G, Held K, Scheffer J, Tenberge KB, Tudzynski P, (2002) CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Molecular Microbiology 46: 305-318.
81. Al-Samarrai TH, Schmid J, (2000) A simple method for extraction of fungal genomic DNA. Lett Appl Microbiol 30: 53-56.
82. Cenis JL, (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20: 2380.
83. Andrie RM, Martinez JP, Ciuffetti LM, (2005) Development of ToxA and ToxB promoter-driven fluorescent protein expression vectors for use in filamentous ascomycetes. Mycologia 97: 1152-1161.
84. Latch GCM, Christensen MJ, (1985) Artificial infections of grasses with endophytes. Ann Appl Biol 107: 17-24.
85. An Z-q, Siegel MR, Hollin W, Tsai H-F, Schmidt D, et al. (1993) Relationships among non-Acremonium sp. fungal endophytes in five grass species. Appl Environ Microbiol 59: 1540-1548.
86. Chung K-R, Schardl CL, (1997) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycol Res 101: 295-301.
87. Panaccione DG, Cipoletti JR, Sedlock AB, Blemings KP, Schardl CL, et al. (2006) Effects of ergot alkaloids on food preference and satiety in rabbits, as assessed with gene-knockout endophytes in perennial ryegrass (Lolium perenne). J Agric Food Chem 54: 4582-4587.
88. Faulkner JR, Hussaini SR, Blankenship JD, Pal S, Branan BM, et al. (2006) On the sequence of bond formation in loline alkaloid biosynthesis. Chembiochem 7: 1078-1088.
89. Spiering MJ, Davies E, Tapper BA, Schmid J, Lane GA, (2002) Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. J Agric Food Chem 50: 5856-5862.
90. Rasmussen S, Lane GA, Mace W, Parsons AJ, Fraser K, et al. (2012) The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. Methods in Molecular Biology 860: 213-226.
91. Farman ML, (2011) Targeted cloning of fungal telomeres. Methods in Molecular Biology 722: 11-31.
92. Huse S, Huber J, Morrison H, Sogin M, D W, (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biology 8: R143.
93. Smit AFA, Hubley R, Green P (1996-2010) RepeatMasker Open-3.0. 3.0 ed: Institute for Syst Biol.
94. Ewing B, Hillier L, Wendl MC, P G, (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8: 175-185.
95. Margolin BS, Garrett-Engele PW, Stevens JN, Fritz DY, Garrett-Engele C, et al. (1998) A methylated Neurospora 5S rRNA pseudogene contains a transposable element inactivated by repeat-induced point mutation. Genetics 149: 1787-1797.
96. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, et al. (2008) MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18: 188-196.
97. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogentic and Genome Res 110: 462-467.
98. Stanke M, Keller O, Gunduz I, Hayes A, Waack S, et al. (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34: W435-W439.
99. Salamov AA, Solovyev VV, (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516-522.
100. Enright AJ, Van Dongen S, Ouzounis CA, (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575-1584.
101. Stein LD, Mungall C, Shu S, Caudy M, Mangone M, et al. (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12: 1599-1610.
102. Donlin MJ (2007) Chapter 9, Unit 9.9: Using the generic genome browser (GBrowse). Current Protocols in Bioinformatics: Wiley Online Library.
103. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M, (2008) Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 18: 1979-1990.
104. Chen F, Mackey AJ, Stoeckert CJ, Roos DS, (2006) OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34: D363-D368.
105. Li L, Stoeckert CJ Jr, Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
106. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
107. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
108. Jothi R, Zotenko E, Tasneem A, Przytycka TM, (2006) COCO-CL: hierarchical clustering of homology relations based on evolutionary correlations. Bioinformatics 22: 779-788.
109. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
110. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
111. Edgar R, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
112. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
113. Anisimova M, Gascuel O, (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55: 539-552.
114. Shimodaira H, Masami H, (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114-1116.
115. Schliep KP, (2011) phangorn: Phylogenetic analysis in R. Bioinformatics 27: 592-593.
116. Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD, (2001) Reverse transcriptase template switching: A SMART (TM) approach for full-length cDNA library construction. Biotechniques 30: 892-897.
117. Wang K, Singh D, Zeng Z, Coleman SJ, Huang Y, et al. (2010) MapSplice: Accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res 38: e178.
118. Young CA, Tapper BA, May K, Moon CD, Schardl CL, et al. (2009) Indole-diterpene biosynthetic capability of epichloë endophytes as predicted by ltm gene analysis. Appl Environ Microbiol 75: 2200-2211.
119. Lorenz N, Olšovská J, Šulc M, Tudzynski P, (2010) Alkaloid cluster gene ccsA of the ergot fungus Claviceps purpurea encodes chanoclavine I synthase, a flavin adenine dinucleotide-containing oxidoreductase mediating the transformation of N-methyl-dimethylallyltryptophan to chanoclavine I. Appl Environ Microbiol 76: 1822-1830.
120. Panaccione DG, Johnson RD, Wang JH, Young CA, Damrongkool P, et al. (2001) Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc Natl Acad Sci U S A 98: 12820-12825.
121. Wang J, Machado C, Panaccione DG, Tsai H-F, Schardl CL, (2004) The determinant step in ergot alkaloid biosynthesis by an endophyte of perennial ryegrass. Fungal Genet Biol 41: 189-198.