The role of host-specificity in the reproductive isolation of Epichloë endophytes revealed by reciprocal infections

Fungal Ecology

Volumn 15, Issue , 2015, Pages 29-38

  Schirrmann, Melanie K ^a   Leuchtmann, Adrian ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Grass endophytes; Host specificity; Hybrids; Reproductive isolation; Speciation

Indexed keywords

ASCOMYCOTA; CLAVICIPITACEAE; DACTYLIS GLOMERATA; HOLCUS LANATUS; POA NEMORALIS;

EID: 84929622874     PISSN: 17545048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funeco.2015.02.004     Document Type: Article

References (53)

1. Brem D., Leuchtmann A. Molecular evidence for host-adapted races of the fungal endophyte Epichloë bromicola after presumed host shifts. Evolution 2003, 57:37-51. 10.2307/3094587.
2. Brosi G.B., McCulley R.L., Bush L.P., Nelson J.A., Classen A.T., Norby R.J. Effects of multiple climate change factors on the tall fescue-fungal endophyte symbiosis: infection frequency and tissue chemistry. New Phytologist 2011, 189:797-805. 10.1111/j.1469-8137.2010.03532.x.
3. Bultman T.L., Leuchtmann A. A test of host specialization by insect vectors as a mechanism for reproductive isolation among entomophilous fungal species. Oikos 2003, 103:681-687. 10.1034/j.1600-0706.2003.12631.x.
4. Bultman T.L., Leuchtmann A., Sullivan T.J., Dreyer A.P. Do Botanophila flies provide reproductive isolation between two species of Epichloë fungi? A field test. New Phytologist 2011, 190:206-212. 10.1111/j.1469-8137.2010.03612.x.
5. Bultman T.L., White J.F., Bowdish T.I., Welch A.M. A new kind of mutualism between fungi and insects. Mycological Research 1998, 102:235-238.
6. Butlin R.K., Debelle A., Kerth C., Snook R.R., Beukeboom L.W., Cajas R.F.C., Diao W., Maan M.E., Paolucci S., Weissing F.J., van de Zande L., Hoikkala A., Geuverink E., Jennings J., Kankare M., Knott K.E., Tyukmaeva V.I., Zoumadakis C., Ritchie M.G., Barker D., Immonen E., Kirkpatrick M., Noor M., Macias Garcia C., Schmitt T., Schilthuizen M., Network M.C.S. What do we need to know about speciation?. Trends in Ecology & Evolution 2012, 27:27-39. 10.1016/j.tree.2011.09.002.
7. Butlin R.K., Galindo J., Grahame J.W. Sympatric, parapatric or allopatric: the most important way to classify speciation?. Philosophical Transactions of the Royal Society of London 2008, 363:2997-3007. 10.1111/j.1558-5646.2007.00091.x.
8. Büker B., Petit E., Begerow D., Hood M.E. Experimental hybridization and backcrossing reveal forces of reproductive isolation in Microbotryum. BMC Evolutionary Biology 2013, 13:224. 10.1186/1471-2148-13-224.10.
9. Christensen M.J. Variation in the ability of Acremonium endophytes of Lolium perenne, Festuca arundinacea and F. pratensis to form compatible associations in the three grasses. Mycological Research 1995, 99:466-470. 10.1016/S0953-7562(09)80647-3.
10. Chung K.R., Hollin W., Siegel M.R., Schardl C.L. Genetics of host specificity in Epichloë typhina. Phytopathology 1997, 87:599-605. 10.1094/PHYTO.1997.87.6.599.
11. Chung K.R., Schardl C.L. Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycological Research 1997, 101:295-301. 10.1017/S0953756296002602.
12. Chung K.R., Schardl C.L. Vegetative compatibility between and within Epichloë species. Mycologia 1997, 89:558-565.
13. Clark E.M., White J.F., Patterson R.M. Improved histochemical techniques for the detection of Acremonium coenophialum in tall fescue and methods of invitro culture of the fungus. Journal of Microbiological Methods 1983, 1:149-155.
14. Clay K. Recent advances in the ecology of endophytes. Proceedings of the Second International Symposium of Acremonium/Grass Interactions. Plenary Papers, Palmerston North, New Zealand 1993, 11-30.
15. Coyne J.A., Orr A. Speciation 2004, Sinauer Associates, Sunderland, MA, USA.
16. Craven K.D., Hsiau P., Leuchtmann A., Hollin W., Schardl C.L. Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden 2001, 88:14-34.
17. De Queiroz K. Species concepts and species delimitation. Systematic Biology 2007, 56:879-886. 10.1080/1063150701701083.
18. Dobzhansky T. Genetics and the Origin of Species 1937, Columbia University Press, New York, NY, USA.
19. Drummond A.J., Ashton B., Buxton S., Cheung M., Duran C., Field M., Heled J., Kearse M., Markowitz S., Moir R., Stones-Havas S., Sturrock S., Thierer T., Wilson A. Geneious v6.1 created by Biomatters 2013, http://www.geneious.com.
20. Giraud T. Speciation in parasites: host switching does not automatically lead to allopatry. Trends in Parasitology 2006, 22:151-152.
21. Giraud T., Refrégier G., Le Gac M., de Vienne D.M., Hood M.E. Speciation in fungi. Fungal Genetics and Biology 2008, 45:791-802. 10.1016/j.fgb.2008.02.001.
22. Glenn A.E., Bacon C.W., Price R., Hanlin R.T. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 1996, 88:369-383.
23. Kohn L.M. Mechanisms of fungal speciation. Annual Review of Phytopathology 2005, 43:279-308. 10.1146/annurev.phyto.43.040204.135958.
24. Latch G., Christensen M.J. Artificial infection of grasses with endophytes. Annals of Applied Biology 1985, 107:17-24.
25. Leuchtmann A. Systematics, distribution, and host specificity of grass endophytes. Natural Toxins 1992, 1:150-162.
26. Leuchtmann A. Isozyme relationships of Acremonium endophytes from twelve Festuca species. Mycological Research 1994, 98:25-33. 10.1016/S0953-7562(09)80331-6.
27. Leuchtmann A. Taxonomy and diversity of Epichloë endophytes. The Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol, and Cultural Impacts 2003, 169-194. Marcel Dekker, New York. J.F. White, C.W. Bacon, N.L. Hywel-Jones, J.W. Spatafora (Eds.).
28. Leuchtmann A., Bacon C.W., Schardl C.L., White J.F., Tadych M. Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 2014, 106:202-215. 10.3852/13-251.
29. Leuchtmann A., Clay K. Isozyme variation in the Acremonium/Epichloë fungal endophyte complex. Phytopathology 1990, 80:1133-1139.
30. Leuchtmann A., Clay K. Nonreciprocal compatibility between Epichloë typhina and four host grasses. Mycologia 1993, 85:157-163.
31. Leuchtmann A., Clay K. The population biology of grass endophytes. The Mycota, Vol. v. Part B: Plant Relationships 1997, 185-202. Springer-Verlag, Berlin, Germany. G.C. Carroll, P. Tudzynski (Eds.).
32. Leuchtmann A., Schardl C.L. Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species. Mycological Research 1998, 102:1169-1182.
33. Leuchtmann A., Schardl C.L., Siegel M.R. Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia 1994, 86:802-812.
34. Leuchtmann A., Steinebrunner F. Evidence for reproductive isolation in Epichloë - a case study. Epichloae, Endophytes of Cool Season Grasses: Implications, Utilization and Biology 2012, 113-116. The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USA. C.A. Young, G.E. Aiken, R.L. McCulley, J.R. Strickland (Eds.).
35. Mallet J. Hybridization as an invasion of the genome. Trends in Ecology & Evolution 2005, 20:229-237. 10.1016/j.tree.2005.02.010.
36. Mayr E. The biological meaning of species. Biological Journal of the Linnean Society 1969, 1:311-320.
37. McNeill J., Barrie F.R., Buck W.R., Demoulin V., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Prado J., Prud'homme van Reine W.F., Smith G.F., Wiersema J.H., Turland N. International Code of Nomenclature for Algae, Fungi and Plants (Melbourne Code) Adopted by the 18th International Botanical Congress Melbourne, Australia 2012, A. R. G. Ganter Verlag, Ruggell.
38. Naffaa W., Astier C., Ravel C., Guillaumin J.J. Creation of stable associations between perennial ryegrass or tall fescue and fungal endophytes. Agronomie 1999, 19:133-144.
39. Peever T.L. Role of host specificity in the speciation of Ascochyta pathogens of cool season food legumes. European Journal of Plant Pathology 2007, 119:119-126. 10.1007/s10658-007-9148-2.
40. Rieseberg L.H., Willis J.H. Plant speciation. Science 2007, 317:910-914.
41. Saikkonen K., Wäli P.R., Helander M. Genetic compatibility determines endophyte-grass combinations. PLoS One 2010, 5:1-6. 10.1371/journal.pone.0011395.g001.
42. Saikkonen K., Wäli P.R., Helander M., Faeth S.H. Evolution of endophyte-plant symbioses. Trends in Plant Science 2004, 9:275-280. 10.1016/j.tplants.2004.04.005.
43. Schardl C.L., Craven K.D. Interspecific hybridization in plant-associated fungi and oomycetes: a review. Molecular Ecology 2003, 12:2861-2873. 10.1046/j.1365-294X.2003.01965.x.
44. Schardl C.L., Leuchtmann A., Chung K.R., Penny D., Siegel M.R. Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Molecular Biology and Evolution 1997, 14:133-143.
45. Schardl C.L., Leuchtmann A., McDonald B.A. Relationships of Epichloë typhina isolates from different host grasses. Proceedings, 6th International Symposium on Fungal Endophytes of Grasses 2007, 451-455. New Zealand Grassland Association (Inc.), Dunedin, New Zealand. A.J. Popay, E.R. Thom (Eds.).
46. Schardl C.L., Leuchtmann A., Spiering M.J. Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 2004, 55:315-340. 10.1146/annurev.arplant.55.031903.141735.
47. Schirrmann M.K., Zoller S., Fior S., Leuchtmann A. Genetic evidence for reproductive isolation among sympatric Epichloë endophytes as inferred from newly developed microsatellite markers. Microbial Ecology 2014, 10.1007/s00248-014-0556-5.
48. Seehausen O., Butlin R.K., Keller I., Wagner C.E., Boughman J.W., Hohenlohe P.A., Peichel C.L., Saetre G.-P., Bank C., Brännström Å., Brelsford A., Clarkson C.S., Eroukhmanoff F., Feder J.L., Fischer M.C., Foote A.D., Franchini P., Jiggins C.D., Jones F.C., Lindholm A.K., Lucek K., Maan M.E., Marques D.A., Martin S.H., Matthews B., Meier J.I., Möst M., Nachman M.W., Nonaka E., Rennison D.J., Schwarzer J., Watson E.T., Westram A.M., Widmer A. Genomics and the origin of species. Nature Reviews Genetics 2014, 15:176-192. 10.1038/nrg3644.
49. Stukenbrock E.H., Bataillon T., Dutheil J.Y., Hansen T.T., Li R., Zala M., McDonald B.A., Wang J., Schierup M.H. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Research 2011, 21:2157-2166. 10.1101/gr.118851.110.
50. Tadych M., Bergen M.S., White J.F. Epichloë spp. associated with grasses: new insights on life cycles, dissemination and evolution. Mycologia 2014, 106:181-201.
51. Western J.H., Cavett J.J. The choke disease of cocksfoot (Dactylis glomerata) caused by Epichloë typhina (Fr.) Tul. Transactions of the British Mycological Society 1959, 42:298-307.
52. White J.F., Bultman T.L. Endophyte-host associations in forage grasses. VIII. Heterothallism in Epichloë typhina. American Journal of Botany 1987, 74:1716-1721.
53. Widmer A., Lexer C., Cozzolino S. Evolution of reproductive isolation in plants. Heredity 2008, 102:31-38. 10.1038/hdy.2008.69.