Plant Systematics and Evolution

, Volume 300, Issue 7, pp 1683–1691 | Cite as

Systemic fungal endophytes and ploidy level in Festuca vivipara populations in North European Islands

  • P. E. GundelEmail author
  • S. Dirihan
  • M. Helander
  • I. Zabalgogeazcoa
  • H. Väre
  • K. Saikkonen
Original Article


Exploring the regional pattern of variation in traits driven by symbiotic interactions may provide insights to understand the evolutionary processes that operate over plant populations. Polyploidy, which is associated with fitness improvement, is expected to increase with latitude and altitude. However, it has never been explored in relation with the occurrence of epichloid fungal endophytes in plants. Both, variation in ploidy level and in the incidence of fungal endophytes, are known to occur in species of fine fescues. Here, we surveyed the occurrence of systemic fungal endophytes in natural Festuca vivipara populations in North European islands. In addition, we identified the fungal species associated with this grass and determined the predominant ploidy level for each population. Endophytes were found in four of six, two of three, and one of three populations for Faroe Islands, Iceland and Great Britain, respectively. With an average low incidence level of 15 % in infected populations, there was no relationship between infection level and either latitude or altitude. The phylogenetic analysis based on sequences ITS and the tub2 genes, supports that the endophytic species is Epichloë festucae, the same as in other fine fescues. We found no variation in ploidy level as all the plants were tetraploid (4X) with 28 chromosomes, a pattern which contrasts with the variation reported in previous antecedents. Our results suggest that apart from low and variable benefits of the endophyte to the plants, there would be a complex dynamics between epichloid endophytes and species of the fine fescue complex which merits further studies.


Pseudovivipary Polyploidy Symbiosis Ecological patterns Epichloë festucae Fine fescues 



We thank Dr. T. Chiurugwi and Professor N.H. Battey because they kindly gave us the plants collected from Great Britain. The research leading to these results has received funding from INTERACT (Grant Agreement No. 262693) under the European Community’s Seventh Framework Programme, and from Academy of Finland (Project No. 137909).


  1. Ahlholm JU, Helander M, Lehtimaki S, Wäli P, Saikkonen K (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183CrossRefGoogle Scholar
  2. Aiken SG, Lefkovitch LP, Darbyshire SJ, Armstrong KC (1988) Vegetative proliferation in inflorescences of red fescue (Festuca rubra s.l, Poaceae). Can J Botany 66(1):1–10CrossRefGoogle Scholar
  3. Bazely DR, Ball JP, Vicari M, Tanentzap AJ, Bérenger M, Rakocevic T, Koh S (2007) Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses in Sweden. Ecography 30:367–374CrossRefGoogle Scholar
  4. Beetle AA (1980) Vivipary, proliferation, and phyllody in grasses. J Range Manage 33:256–261CrossRefGoogle Scholar
  5. Brochmann C, Brysting AK, Alasos IG, Borgen L, Grundt HH, Scheen A-C, Elven R (2004) Polyploidy in arctic plants. Biol J Linn Soc 82:521–536CrossRefGoogle Scholar
  6. Bultman TL, White JF Jr (1988) Pollination of a fungus by a fly. Oecologia 75(2):317–319CrossRefGoogle Scholar
  7. Byrd AD, Schardl CL, Songlin PJ, Mogen KL, Siegel MR (1990) The b-tubulin gene of Epichloë typhina from perennial ryegrass (Lolium perenne). Curr Genet 18:347–354PubMedCrossRefGoogle Scholar
  8. Chiurugwi T, Beaumont MA, Wilkinson MJ, Battey NH (2011) Adaptive divergence and speciation among sexual and pseudoviviparous populations of Festuca. Heredity 106:854–861PubMedCentralPubMedCrossRefGoogle Scholar
  9. Clay K (1986) Induced vivipary in the sedge Cyperus virens and the transmission of the fungus Balansia cyperi (Clavicipitaceae). Can J Bot 64:2984–2988CrossRefGoogle Scholar
  10. Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127PubMedCrossRefGoogle Scholar
  11. Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL (2001) Multigene phylogeny of Epichloe species, fungal symbionts of grasses. Ann Mo Bot Gard 88(1):14–34CrossRefGoogle Scholar
  12. Darlington CD, La Cour F (1969) The handling of chromosomes. Allen & Unwin, LondonGoogle Scholar
  13. Dolezel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2(9):2233–2244PubMedCrossRefGoogle Scholar
  14. Elmqvist T, Cox PA (1996) The evolution of vivipary in flowering plants. Oikos 77(1):3–9CrossRefGoogle Scholar
  15. Elven R (2005) Norsk Flora. Det Norske Samlaget, Oslo 1230 pGoogle Scholar
  16. Flovik K (1938) Cytological studies of arctic grasses. Hereditas 24(3):266–377Google Scholar
  17. Gould FW, Shaw RB (1983) Grass Systematics, 2nd edn. Texas A&M University Press, College StationGoogle Scholar
  18. Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T (2007) Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients. Ecography 30:422–430CrossRefGoogle Scholar
  19. Gundel PE, Batista WB, Texeira M, Martínez-Ghersa MA, Omacini M, Ghersa CM (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. P Roy Soc B-Biol Sci 275:897–905CrossRefGoogle Scholar
  20. Gundel PE, Martínez-Ghersa MA, Batista WB, Ghersa CM (2010) Dynamics of Neotyphodium endophyte infection in ageing seed pools: incidence of differential viability loss of endophyte, infected seed, and non-infected seed. Ann Appl Biol 156(2):199–209CrossRefGoogle Scholar
  21. Gundel PE, Rudgers JA, Ghersa CM (2011) Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos 120(8):1121–1128CrossRefGoogle Scholar
  22. Harmer R, Lee JA (1978) The Germination and viability of Festuca vivipara (L.) Sm. plantlets. New Phytol 81:745–751CrossRefGoogle Scholar
  23. Heide OM (1988) Environmental modification of flowering and viviparous proliferation in Festuca vivipara and Festuca ovina. Oikos 51:171–178CrossRefGoogle Scholar
  24. Iannone LJ, Novas MV, Young CA, De Battista JP, Schardl CL (2012) Endophytes of native grasses from South America: biodiversity and ecology. Fungal Ecology 5:357–363CrossRefGoogle Scholar
  25. Jauhar PP (1993) Cytogenetics of the Festuca-Lolium Complex: Relevance to Breeding (Monographs on Theoretical and Applied Genetics). Springer-Verlag, Berlin HeidelbergGoogle Scholar
  26. Lee JA, Harmer R (1980) Vivipary, a reproductive strategy in response to environmental stress? Oikos 35(2):254–265CrossRefGoogle Scholar
  27. Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82(4):651–663CrossRefGoogle Scholar
  28. Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1:150–162PubMedCrossRefGoogle Scholar
  29. Leuchtmann A, Schardl CL, Siegel MR (1994) Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia 86:802–812CrossRefGoogle Scholar
  30. Löve Á, Löve D (1956) Cytotaxonomical conspectus of the Icelandic flora. Acta Horti Gothob 20:65–291Google Scholar
  31. Löve Á, Löve D (1961) Chromosome numbers of central and northwest European plants species. Opera Botanica 5:1–581Google Scholar
  32. Pils G (1985) Das Festuca vivipara-Problem in den Alpen. Plant Syst Evol 149:19–45CrossRefGoogle Scholar
  33. Rønning OI (1996) The flora of Svalbard. Polar Handbook 9. Norsk Polarinstitutt, Oslo. p 184Google Scholar
  34. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  35. Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23:360–366CrossRefGoogle Scholar
  36. Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapopulations. P Roy Soc B-Biol Sci 269:1397–1403CrossRefGoogle Scholar
  37. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedCrossRefGoogle Scholar
  38. Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113CrossRefGoogle Scholar
  39. Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195Google Scholar
  40. Sarapul’tsev IE (2001) The phenomenon of Pseudoviviparity in Alpine and Arctomontane grasses (Deschampsia Beauv., Festuca L., and Poa L.). Ekologiya (from Russian Journal of Ecology) 3:188–196Google Scholar
  41. Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol 33:69–82PubMedCrossRefGoogle Scholar
  42. Schardl CL (2010) The Epichloae, symbionts of the grass subfamily Poöideae. Ann Mo Bot Gard 97(4):646–665CrossRefGoogle Scholar
  43. Schardl CL, Leuchtmann A, Tsai H-F, Collett MA, Watt DM, Scott DB (1994) Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloe typhina. Genetics 136:1307–1317PubMedCentralPubMedGoogle Scholar
  44. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269CrossRefGoogle Scholar
  45. Šmarda P, Kočí K (2003) Chromosome number variability in Central European members of the Festuca ovina and F. pallens groups (Sect. Festuca). Folia Geobot 38:65–95CrossRefGoogle Scholar
  46. Šmarda P, Bureš P, Horová L, Foggi B, Rossi G (2008) Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction. Ann Bot-London 101:421–433Google Scholar
  47. Tadych M, Bergen M, Dugan FM, White JF Jr (2007) Evaluation of the potential role of water in spread of conidia of the Neotyphodium endophyte of Poa ampla. Mycol Res 111:466–472PubMedCrossRefGoogle Scholar
  48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  49. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882CrossRefGoogle Scholar
  50. Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22(3):120–126PubMedCrossRefGoogle Scholar
  51. Tredway LP, White JF Jr, Gaut BS, Reddy PV, Richardson MD, Clarke BB (1999) Phylogenetic relationships within and between Epichloë and Neotyphodium endophytes as estimated by AFLP markers and rDNA sequences. Mycol Res 103(12):1593–1603CrossRefGoogle Scholar
  52. (2013) Missouri Botanical Garden. © Missouri Botanical Garden—4344 Shaw Boulevard—Saint Louis, Missouri 63110
  53. Tyler B, Borrill M, Chorlton K (1978) Studies in Festuca. X. Observations on germination and seedling cold tolerance in diploid Festuca pratensis and tetraploid F. pratensis var. Apennina in relation to their altitudinal distribution. J Appl Ecol 15(1):219–226CrossRefGoogle Scholar
  54. Väre H, Partanen R (2012) Suomen tunturikasvio, Finnish field flora, 2nd edn. Metsäkustannus, Helsinki, p 256Google Scholar
  55. Wäli PR, Ahlholm JU, Helander M, Saikkonen K (2007) Occurrence and genetic structure of the systemic grass endophyte Epichloë festucae in fine fescue populations. Microb Ecol 53:20–29PubMedCrossRefGoogle Scholar
  56. Watson PJ (1958) The distribution in Britain of diploid and tetraploid races within the Festuca ovina group. New Phytol 57(1):11–18CrossRefGoogle Scholar
  57. White JF Jr, Cole GT (1986) Endophyte-host associations in forage grasses. V. Occurrence of fungal endophytes in certain species of Bromus and Poa. Mycologia 78:846–850CrossRefGoogle Scholar
  58. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfland DH, Sninsky JJ, White TS (eds) PCR protocols. A guide to methods and applications. Academic Press, Waltham, pp 315–322Google Scholar
  59. Wilkinson MJ, Stace CA (1991) A new taxonomic treatment of the Festuca ovina L aggregate (Poaceae) in the British Isles. Bot J Linn Soc 106:347–397CrossRefGoogle Scholar
  60. Zabalgogeazcoa I, Romo M, Keck E, Vázquez de Aldana BR, García Ciudad A, García Criado B (2006) The infection of Festuca rubra subsp. pruinosa by Epichloë festucae. Grass Forage Sci 61:71–76CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • P. E. Gundel
    • 1
    • 2
    Email author
  • S. Dirihan
    • 1
    • 3
  • M. Helander
    • 3
  • I. Zabalgogeazcoa
    • 4
  • H. Väre
    • 5
  • K. Saikkonen
    • 1
  1. 1.Department of Plant ProductionMTT Agrifood Research FinlandJokioinenFinland
  2. 2.IFEVA-CONICET, Faculty of AgronomyBuenos Aires University (UBA)Buenos AiresArgentina
  3. 3.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  4. 4.Instituto de Recursos Naturales y AgrobiologíaCSICSalamancaSpain
  5. 5.Finnish Museum of Natural History, Botanical MuseumUniversity of HelsinkiHelsinkiFinland

Personalised recommendations