Genetic diversity in epichloid endophytes of Hordelymus europaeus suggests repeated host jumps and interspecific hybridizations

Molecular Ecology

Volumn 21, Issue 11, 2012, Pages 2713-2726

  Oberhofer, Martina ^a   Leuchtmann, Adrian ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

endophytic fungi; interspecific hybrids; Neotyphodium; phylogeography; symbiosis

Indexed keywords

ARTICLE; CHIMERA; ENDOPHYTE; EPICHLOE; EUROPE; GENETIC VARIABILITY; GENETICS; HAPLOIDY; MICROBIOLOGY; MOLECULAR GENETICS; NEOTYPHODIUM; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT SEED; PLOIDY; POACEAE; REPRODUCTION; SYMBIOSIS;

CHIMERA; ENDOPHYTES; EPICHLOE; EUROPE; GENETIC VARIATION; HAPLOIDY; MOLECULAR SEQUENCE DATA; NEOTYPHODIUM; PHYLOGENY; PLOIDIES; POACEAE; REPRODUCTION; SEEDS; SYMBIOSIS;

EPICHLOE; FUNGI; HORDELYMUS EUROPAEUS; NEOTYPHODIUM;

EID: 84861553317     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05459.x     Document Type: Article

References (66)

1. Amalric C, Sallanon H, Monnet F, Hitmi A, Coudret A, (1999) Gas exchange and chlorophyll fluorescence in symbiotic and non-symbiotic ryegrass under water stress. Photosynthetica, 37, 107-112.
2. Baltisberger M, Leuchtmann A, (1991) Investigations on some Gramineae from Albania and Greece (chromosome numbers and endophyte infection). Berichte Geobotanisches Institut ETH, Stiftung Rübel, 57, 182-192.
3. Brasier C, (2000) The rise of the hybrid fungi. Nature, 405, 134-135.
4. Braun-Blanquet J, (1964) Pflanzensoziologie: Grundzüge der Vegetationskunde, 3rd edn. Springer Verlag, Wien.
5. Brem D, Leuchtmann A, (2003) Molecular evidence for host-adapted races of the fungal endophyte Epichloë bromicola after presumed host shifts. Evolution, 57, 37-51.
6. Brunet J, (1993) Environmental and histochemical factors limiting the distribution of rare forest grasses in South Sweden. Forest Ecology and Management, 61, 263-275.
7. Burnett JH, (2003) Fungal Populations and Species. Oxford University Press, Oxford, UK.
8. Chen YG, Ji YL, Yu HS, Wang ZW, (2009) A new Neotyphodium species from Festuca parvigluma Steud. grown in China. Mycologia, 101, 681-685.
9. Chung KR, Schardl CL, (1997) Vegetative compatibility between and within Epichloë species. Mycologia, 89, 558-565.
10. Chung KR, Hollin W, Siegel MR, Schardl CL, (1997) Genetics of host specificity in Epichloë typhina. Phytopathology, 87, 599-605.
11. Clay K, (1990) Fungal endophytes of grasses. Annual Review of Ecology and Systematics, 21, 275-297.
12. Clay K, Schardl CL, (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. The American Naturalist, 160, 99-127.
13. Clay K, Holah J, Rudgers JA, (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proceedings of the National Academy of Sciences of the United States of America, 102, 12465-12470.
14. Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL, (2001) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden, 88, 14-34.
15. Dvořáková H, Fér T, Marhold K, (2010) Phylogeographic pattern of the European forest grass species Hordelymus europaeus: cpDNA evidence. Flora, 205, 418-423.
16. Ehrendorfer F, (1980) Polyploidy and Distribution. Plenum Press, New York.
17. Gentile A, Rossi MS, Cabral D, Craven KD, Schardl CL, (2005) Origin, divergence, and phylogeny of Epichloë endophytes of native Argentine grasses. Molecular Phylogenetics and Evolution, 35, 196-208.
18. Ghimire SR, Rudgers JA, Charlton ND, Young C, Craven KD, (2011) Prevalence of an intraspecific Neotyphodium hybrid in natural populations of stout wood reed (Cinna arundinacea L.) from eastern North America. Mycologia, 103, 75-84.
19. Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME, (2008) Speciation in fungi. Fungal Genetics and Biology, 45, 791-802.
20. Gonthier DJ, Sullivan TJ, Brown KL, et al. (2008) Stroma-forming endophyte Epichloë glyceriae provides wound-inducible herbivore resistance to its grass host. Oikos, 117, 629-633.
21. Graae BJ, (2002) The role of epizoochorous seed dispersal of forest plant species in a fragmented landscape. Seed Science Research, 12, 113-120.
22. Gugerli F, Sperisen C, Büchler U, et al. (2001) Haplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western Alps. Molecular Ecology, 10, 1255-1263.
23. Hamilton CE, Dowling TE, Faeth SH, (2010) Hybridization in endophyte symbionts alters host response to moisture and nutrient treatments. Microbial Ecology, 59, 768-775.
24. Hewitt GM, (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
25. Iannone LJ, Cabral D, Schardl CL, Rossi MS, (2009) Phylogenetic divergence, morphological and physiological differences distinguish a new Neotyphodium endophyte species in the grass Bromus auleticus from South America. Mycologia, 101, 340-351.
26. Kuldau GA, Tsai HF, Schardl CL, (1999) Genome sizes of Epichloë species and anamorphic hybrids. Mycologia, 91, 776-782.
27. Leuchtmann A, (1992) Systematics, distribution, and host specificity of grass endophytes. Natural Toxins, 1, 150-162.
28. Leuchtmann A, (1994) Isozyme relationships of Acremonium endophytes from 12 Festuca species. Mycological Research, 98, 25-33.
29. Leuchtmann A, (2003) Taxonomy and diversity of Epichloë endophytes. In: Clavicipitalean Fungi (eds, White JF, Bacon C, Hywel-Jones NL, Spatafora JW,), pp. 169-193. Marcel Dekker, New York.
30. Leuchtmann A, Schardl CL, Siegel MR, (1994) Sexual compatibilities and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia, 86, 802-812.
31. Maddison DR, Maddison WP, (2005) MacClade 4: Analyses of Phylogeny and Character Evolution. Sinauer Associates, Sunderland, Massachusetts.
32. Mizianty M, Frey L, Bieniek W, Boroń P, Szklarczyk M, (2007) Variability and structure of natural populations of Hordelymus europaeus (L.) Jess. ex Harz and Leymus arenarius (L.) Hochst. as revealed by morphology and DNA markers. Plant Systematics and Evolution, 269, 15-28.
33. Moon CD, Scott B, Schardl CL, Christensen MJ, (2000) The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia, 92, 1103-1118.
34. Moon CD, Miles CO, Järlfors U, Schardl CL, (2002) The evolutionary origins of three new Neotyphodium endophyte species from grasses indigenous to the Southern Hemisphere. Mycologia, 94, 694-711.
35. Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL, (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Molecular Ecology, 13, 1455-1467.
36. Muller HJ, (1964) The relation of recombination to mutational advance. Mutation Research, 1, 2-9.
37. Ni Y, Asamoah-Odei N, Sun G, (2011) Maternal origin, genome constitution and evolutionary relationships of polyploid Elymus species and Hordelymus europaeus. Biologia Plantarum, 55, 68-74.
38. Omacini M, Chaneton EJ, Bush L, Ghersa CM, (2009) A fungal endosymbiont affects host plant recruitment through seed- and litter-mediated mechanisms. Functional Ecology, 23, 1148-1156.
39. Petersen G, Seberg O, (2008) Phylogenetic relationships of allotetraploid Hordelymus europaeus (L.) Harz (Poaceae: Triticeae). Plant Systematics and Evolution, 273, 87-95.
40. Petit RJ, Aguinagalde I, de Beaulieu JL, et al. (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300, 1563-1565.
41. Posada D, (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
42. Provan J, Bennett KD, (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564-571.
43. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
44. Schardl CL, Craven KD, (2003) Interspecific hybridization in plant-associated fungi and oomycetes: a review. Molecular Ecology, 12, 2861-2873.
45. Schardl CL, Leuchtmann A, Tsai HF, et al. (1994) Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics, 136, 1307-1317.
46. Schardl CL, Leuchtmann A, Chung KR, Penny D, Siegel MR, (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Molecular Biology and Evolution, 14, 133-143.
47. Schardl CL, Leuchtmann A, Spiering MJ, (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology, 55, 315-340.
48. Schardl CL, Leuchtmann A, McDonald BA, (2007) Relationships of Epichloë typhina isolates from different host grasses. In: Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses (eds, Popay AJ, Thom ER,), pp. 451-455. New Zealand Grassland Association (Inc.), Dunedin, New Zealand.
49. Schardl CL, Craven KD, Speakman S, et al. (2008) A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses. Systematic Biology, 57, 483-498.
50. Soltis DE, Haufler CH, Darrow DC, Gastony GJ, (1983) Starch gel electrophoresis of ferns-a compilation of grinding buffers, gel and electrode buffers, and staining schedules. American Fern Journal, 73, 9-27.
51. Stewart JR, Lister AM, (2001) Cryptic northern refugia and the origins of the modern biota. Trends in Ecology & Evolution, 16, 608-613.
52. Stöhr O, (2000) Glyceria striata (Lam.) Hitchc.-neu für Salzburg sowie weitere interessante Gefäßpflanzenfunde für dieses Bundesland. Linzer Biologische Beiträge, 32, 329-340.
53. Sullivan TJ, Faeth SH, (2004) Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica. Molecular Ecology, 13, 649-656.
54. Sullivan TJ, Faeth SH, (2008) Local adaptation in Festuca arizonica infected by hybrid and nonhybrid Neotyphodium endophytes. Microbial Ecology, 55, 697-704.
55. Swofford DL, (2003) PAUP: Phylogenetic Analysis Using Parsimony and Other Methods. Sinauer Associates, Sunderland, Massachusetts, USA.
56. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
57. Thompson JD, Lumaret R, (1992) The evolutionary dynamics of polyploid plants-origins, establishment and persistence. Trends in Ecology & Evolution, 7, 302-307.
58. Tsai HF, Liu JS, Staben C, et al. (1994) Evolutionary diversification of fungal endophytes of tall festuce grass by hybridization with Epichloë species. Proceedings of the National Academy of Sciences of the United States of America, 91, 2542-2546.
59. Tutin TG, (1980) Flora Europaea. Cambridge University Press, Cambridge, UK.
60. Vershinin A, Svitashev S, Gummesson PO, et al. (1994) Characterization of a family of tandemly repeated DNA-sequences in Triticaceae. Theoretical and Applied Genetics, 89, 217-225.
61. Vonbothmer R, Jacobsen N, (1989) Intergeneric hybridization between Hordeum and Hordelymus (Poaceae). Nordic Journal of Botany, 9, 113-117.
62. Vonbothmer R, Lu BR, Lindelaursen I, (1994) Intergeneric hybridization and C-banding patterns in Hordelymus (Triticaceae, Poaceae). Plant Systematics and Evolution, 189, 259-266.
63. Wäli PR, Helander M, Nissinen O, Lehtonen P, Saikkonen K, (2008) Endophyte infection, nutrient status of the soil and duration of snow cover influence the performance of meadow fescue in sub-arctic conditions. Grass and Forage Science, 63, 324-330.
64. Yan K, Yanling J, Xianghui S, et al. (2009) Taxonomy of Neotyphodium endophytes of Chinese native Roegneria plants. Mycologia, 101, 211-219.
65. Zhang X, Ren AZ, Ci HC, Gao YB, (2010) Genetic diversity and structure of Neotyphodium species and their host Achnatherum sibiricum in a natural grass-endophyte system. Microbial Ecology, 59, 744-756.
66. Zwickl DJ, (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Dissertation, University of Texas, Austin, Texas, USA.