Phylogenomics of asexual Epichloë fungal endophytes forming associations with perennial ryegrass

BMC Evolutionary Biology

Volumn 15, Issue 1, 2015, Pages

  Hettiarachchige, Inoka K ^a,b,c   Ekanayake, Piyumi N ^a,c   Mann, Ross C ^a,c   Guthridge, Kathryn M ^a,c   Sawbridge, Timothy I ^a,c   Spangenberg, German C ^a,b,c   Forster, John W ^a,b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c University of Melbourne   (Australia)

Author keywords

Mating type; Nuclear gene; Pasture grass; Progenitor; Taxonomy; Whole genome sequencing

Indexed keywords

ENDOPHYTE; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; FUNGUS; GENE EXPRESSION; GENETIC MARKER; GENOMICS; GRASS; MOLECULAR ANALYSIS; MUTUALISM; PASTURE; PERENNIAL PLANT; PHYLOGENETICS; TAXONOMY;

LOLIUM PERENNE; PERA;

ELONGATION FACTOR 1; FUNGAL PROTEIN; FUSED HETEROCYCLIC RINGS; PERAMINE; POLYAMINE; TUBULIN;

CLASSIFICATION; ENDOPHYTE; EPICHLOE; FUNGAL MATING TYPE GENE; GENETICS; LOLIUM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS;

ENDOPHYTES; EPICHLOE; FUNGAL PROTEINS; GENES, MATING TYPE, FUNGAL; HETEROCYCLIC COMPOUNDS, 2-RING; LOLIUM; PEPTIDE ELONGATION FACTOR 1; PHYLOGENY; POLYAMINES; SYMBIOSIS; TUBULIN;

EID: 84938990296     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-015-0349-6     Document Type: Article

References (52)

1. 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. International Journal of Evolutionary Biology 2011: Article ID 921312, 11 pages, doi:10.4061/2011/921312.
2. Khan A, Bassett S, Voisey C, Gaborit C, Johnson L, Christensen M, et al. Gene expression profiling of the endophytic fungus Neotyphodium lolii in association with its host plant perennial ryegrass. Australas Plant Pathol. 2010;39(5):467-76.
3. Cunningham PJ, Blumenthal MJ, Anderson MW, Prakash KS, Leonforte A. Perennial ryegrass improvement in Australia. New Zealand J Agric Res. 1994;37(3):295-310.
4. Sampoux JP, Baudouin P, Bayle B, Béguier V, Bourdon P, Chosson JF, et al. Breeding perennial ryegrass (Lolium perenne L.) for turf usage: an assessment of genetic improvements in cultivars released in Europe, 1974-2004. Grass and Forage Sci. 2013;68(1):33-48.
5. Posselt UK, Barre P, Brazauska G, Turner LB. Comparative analysis of genetic similarity between perennial ryegrass genotypes investigated with AFLPs, ISSRs, RAPDs and SSRs. Czech J Genet Plant Breeding. 2006;42(3):87-94.
6. Card SD, Rolston MP, Lloyd-West C, Hume DE. Novel perennial ryegrass-Neotyphodium endophyte associations: relationships between seed weight, seedling vigour and endophyte presence. Symbiosis. 2014;62(1):51-62.
7. Felitti S, Shields K, Ramsperger M, Tian P, Sawbridge T, Webster T, et al. Transcriptome analysis of Neotyphodium and Epichloë grass endophytes. Fungal Genet Biol. 2006;43(7):465-75.
8. Leuchtmann A, Bacon CW, Schardl CL, White JJF, Tadych M. Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia. 2014;106(2):202-15.
9. Rodriguez RJ, White Jr JF, Arnold AE SRR. Fungal endophytes: diversity and functional roles. New Phytologist. 2009;182(2):314-30.
10. Schardl CL, Young CA, Faulkner JR, Florea S, Pan J. Chemotypic diversity of Epichloë, fungal symbionts of grasses. Fungal Ecol. 2012;5(3):331-44.
11. van Zijll de Jong E, Dobrowolski MP, Sandford A, Smith KF, Willocks MJ, Spangenberg GC, et al. Detection and characterisation of novel fungal endophyte genotypic variation in cultivars of perennial ryegrass (Lolium perenne L.). Aust J Agr Res. 2008;59(3):214-21.
12. Yan K, Yanling J, Kunran Z, Hui W, Huimin M, Zhiwei W. A new Epichloë species with interspecific hybrid origins from Poa pratensis ssp. pratensis in Liyang, China. Mycologia. 2011;103(6):1341-50.
13. Siegel MR, Latch GCM, Johnson MC. Fungal endophytes of grasses. Annu Rev Phytopathol. 1987;25:293-315.
14. Schardl CL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol. 2004;55:315-40.
15. Ravel C, Courty C, Coudret A, Charmet G. Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie. 1997;17(3):173-81.
16. Malinowski DP, Belesky DP. Tall fescue aluminum tolerance is affected by Neotyphodium coenophialum endophyte. J Plant Nutr. 1999;22(8):1335-49.
17. Rowan DD, Gaynor DL. Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. J Chem Ecol. 1986;12(3):647-58.
18. Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL. Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol Plant Microbe Interact. 2000;13(10):1027-33.
19. Yates SG, Plattner RD, Garner GB. Detection of ergopeptine alkaloids in endophyte infected, toxic Ky-31 tall fescue by mass spectrometry/mass spectrometry. J Agric Food Chem. 1985;33:719-22.
20. Scott B, Schardl CL. Fungal symbionts of grasses: evolutionary insights and agricultural potential. Trends Microbiol. 1993;1(5):196-200.
21. West CP. Physiology and drought tolerance of endophyte-infected grasses. In: Bacon CW, White JF, editors. Biotechnology of endophytic fungi of grasses. Boca Raton, FL: CRC Press; 1994. p. 87-99.
22. Latch GCM, Christensen MJ, Samuels GJ. Five endophytes of Lolium and Festuca in New Zealand. Mycotaxon. 1984;20:535-50.
23. 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):1083-92.
24. 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):1307-17.
25. Moon CD, Guillaumin J, Ravel C, Li C, Craven KD, Schardl CL. New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae. Mycologia. 2007;99(6):895-905.
26. Moon CD, Scott B, Schardl CL, Christensen MJ. The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia. 2000;92(6):1103-18.
27. Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GC, Siegel MR, et al. Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci U S A. 1994;91(7):2542-6.
28. Ghimire SR, Rudgers JA, Charlton ND, Young C, Craven KD. Prevalence of an intraspecific Neotyphodium hybrid in natural populations of stout wood reed (Cinna arundinacea L.) from eastern North America. Mycologia. 2011;103(1):75-84.
29. Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL. Multigene phylogeny of Epichloe species, fungal symbionts of grasses. Ann Mo Bot Gard. 2001;88(1):14-34.
30. Ekanayake P, Rabinovich M, Guthridge KM, Spangenberg GC, Forster JW, Sawbridge T. Phylogenomics of fescue grass-derived fungal endophytes based on selected nuclear genes and the mitochondrial gene complement. BMC Evol Biol. 2013;13(1):270.
31. Takach JE, Mittal S, Swoboda GA, Bright SK, Trammell MA, Hopkins AA, et al. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl Environ Microbiol. 2013;78(16):5501-10.
32. Moon CD, Miles C, 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.
33. Moon CD, Tapper BA, Scott B. Identification of Epichloë endophytes in planta by a microsatellite-based PCR fingerprinting assay with automated analysis. Appl Environ Microbiol. 1999;65(3):1268-79.
34. van Zijll de Jong E, Guthridge KM, Spangenberg GC, Forster JW. Development and characterization of EST-derived simple sequence repeat (SSR) markers for pasture grass endophytes. Genome. 2003;46(2):277-90.
35. Kaur J, Ekanayake P, Tian P, van Zijll de Jong E, Dobrowolski MP et al. Discovery and characterization of novel asexual Epichloë endophytes from perennial ryegrass (Lolium perenne L.). Crop Pasture Sci., accepted subject to minor revision and resubmitted.
36. 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;52:2243-52.
37. Rocak S, Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol. 2004;5:232-41.
38. Palomares-Rius J, Hirooka Y, Tsai I, Masuya H, Hino A, Kanzaki N, et al. Distribution and evolution of glycoside hydrolase family 45 cellulases in nematodes and fungi. BMC Evol Biol. 2014;14(1):69.
39. López-Berges MS, Rispail N, Prados-Rosales RC, Pietro AD. A nitrogen response pathway regulates virulence in plant pathogenic fungi. Plant Signal Behav. 2010;5(12):1623-5.
40. van Zijll de Jong E, Dobrowolski MP, Bannan NR, Stewart AV, Smith KF, Spangenberg GC, et al. Global genetic diversity of the perennial ryegrass fungal endophyte Neotyphodium lolii. Crop Sci. 2008;48:1487-501.
41. Davidson SE, Sawbridge TI, Rabinovich M, Kaur J, Forster JW, Guthridge KM et al. Pan-Genome analysis of perennial ryegrass endophytes. In: Proceedings of the 7th International Symposium on the Molecular Breeding of Forage and Turf 2012' Salt Lake City, UT (Eds BS Bushman, GC Spangenberg) p 80 (MBFT Organizing Committee) 2012.
42. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST - A new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389-402.
43. Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, et al. Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci. PLoS Genet. 2013;9(2):e1003323.
44. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821-9.
45. 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(10):2731-9.
46. Clay K, Schardl S. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat. 2002;160:S99-127.
47. 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.
48. Schardl CL. The Epichloë, symbionts of the grass subfamily Poöideae. Ann Mo Bot Gard. 2010;97(4):646-65.
49. Gadagkar SR, Rosenberg MS, Kumar S. Inferring species phylogenies from multiple genes: concatenated sequence tree versus consensus gene tree. J Exp Zool B Mol Dev Evol. 2005;304B(1):64-74.
50. Tian P, Kaur J, Guthridge KM, Rochfort S, Forster JW, Spangenberg GC. Metabolome analysis of symbiota established with novel Neotyphodium endophytes in a diverse panel of isogenic perennial ryegrass host genotypes In: Proceedings of the 7th International Symposium on the Molecular Breeding of Forage and Turf 2012' Salt Lake City, UT (Eds BS Bushman, GC Spangenberg) p 112 (MBFT Organizing Committee) 2012
51. Kaur J, Ekanayake PN, Rabinovich M, Ludlow EJ, Tian P, Rochfort S et al. Analysis of compatibility and stability in designer endophyte-grass associations between perennial ryegrass and Neotyphodium species. In 'Proceedings of the 7th International Symposium on the Molecular Breeding of Forage and Turf 2012' Salt Lake City, UT (Eds BS Bushman, GC Spangenberg) p 73 (MBFT Organizing Committee) 2012.
52. Hettiarachchige I, Ekanayake PN, Mann RC, Guthridge KM, Sawbridge TI, Spangenberg GC et al. TreeBASE 2015. http://purl.org/phylo/treebase/phylows/study/TB2:S17154.