Skip to main content
Log in

Imperfect Vertical Transmission of the Endophyte Neotyphodium in Exotic Grasses in Grasslands of the Flooding Pampa

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Cool-season grasses establish symbioses with vertically transmitted Neotyphodium endophytes widespread in nature. The frequency of endophyte-infected plants in closed populations (i.e., without migrations) depends on both the differential fitness between infected and non-infected plants, and the endophyte-transmission efficiency. Most studies have been focused on the first mechanism ignoring the second. Infection frequency and endophyte transmission from vegetative tissues to seeds were surveyed in two grasses growing in vegetation units that differ in flood and grazing regimes, and soil salinity. Transmission efficiency and infection frequency for tall fescue did not vary significantly and were 0.98 and 1.00, respectively. For Italian ryegrass, transmission efficiency and infection frequency were 0.88 and 0.57 in humid prairies, and 0.96 and 0.96 in the other vegetation units. Only in humid mesophytic meadows, the observed pattern was irrespective of the presence or absence of grazers. Our results suggest that selection forces for endophyte infection are different for both species. Imperfect transmission was only compensated in tall fescue through an increased fitness of infected plants. Interpreting variations of infection frequency only in terms of differential fitness can be misleading, considering that endophyte transmission can be imperfect and variable in nature. Therefore, this study highlights the importance of measuring transmission efficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Afkhami ME, Rudgers JA (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am Nat 172:405–416

    Article  PubMed  Google Scholar 

  2. Aragón R, Oesterheld M (2008) Linking vegetation heterogeneity and functional attributes of temperate grasslands through remote sensing. Appl Veg Sci 11:115–128

    Article  Google Scholar 

  3. Bacon CW, White JF Jr (1994) Stains, media, and procedures for analyzing endophytes. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC, Boca Raton, FL, pp 47–56

    Google Scholar 

  4. 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. Ecography 30(3):367–374

    Article  Google Scholar 

  5. Canals RM, San Emeterio L, Oreja A (2008) Chances of loss of fungal endophytes in agronomic grasses: A case-study for Lolium rigidum. Agric Ecosyst Environ 127:146–152

    Article  Google Scholar 

  6. Chaneton EJ, Perelman SB, Omacini M, León RJC (2002) Grazing, environmental heterogeneity, and alien plant invasions in temperate Pampa grasslands. Biol Invasions 4:7–24

    Article  Google Scholar 

  7. Cheplick GP (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exper Bot 60:202–210

    Article  Google Scholar 

  8. Clay K (1993) The ecology and evolution of endophytes. Agric Ecosyst Environ 44:39–64

    Article  Google Scholar 

  9. Clay K, Schardl C (2002) Evolutionary origin and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127

    Article  Google Scholar 

  10. Clay K, Holah J, Rudgers JR (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. PNAS 102(35):12465–12470

    Article  PubMed  CAS  Google Scholar 

  11. Clement SL, Elberson LR, Kynaston M (2007) High Neotyphodium infection frequencies in tillers and seed of infected wild fescue plants. In: Popay AJ, Thom ER (eds) Proc. of the 6th International Symposium on Fungal Endophytes of Grasses, “From Lab To Farm”. New Zealand Grassland Association, New Zealand, pp 49–42

    Google Scholar 

  12. Darby AC, Douglas AE (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Appl Environ Microbiol 69:4403–4407

    Article  PubMed  CAS  Google Scholar 

  13. Dawson K, Veblen K, Young T (2007) Experimental evidence for an alkali ecotype of Lolium multiflorum, an exotic invasive annual grass in the Central Valley, CA, USA. Biol Invasions 9:327–334

    Article  Google Scholar 

  14. De Battista JP (2005) Neotyphodium research and application: current trends in South America. In: Roberts C, West CP, Spiers D (eds) Neotyphodium in cool-season grasses. Blackwell, Oxford, p 65–71

    Chapter  Google Scholar 

  15. Douglas AE (1994) Symbiotic interactions. Oxford University Press, Oxford, UK

    Google Scholar 

  16. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603

    Article  Google Scholar 

  17. Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98:25–36

    Article  Google Scholar 

  18. Faeth SH, Hamilton CE (2006) Does an asexual endophyte symbiont alter life stage and long-term survival in a perennial host grass? Microb Ecol 52:748–755

    Article  PubMed  Google Scholar 

  19. 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(3):422–430

    Google Scholar 

  20. 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. Proc R Soc Lond B 275:897–905

    Article  Google Scholar 

  21. Gwinn KD, Fribourg HA, Waller JC, Saxton AM, Smith MC (1998) Changes in Neotyphodium coenophialum infestation levels in tall fescue pastures due to different grazing pressures. Crop Sci 38:201–204

    Google Scholar 

  22. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. TREE 14(2):49–53

    PubMed  Google Scholar 

  23. Hill NS, Bouton JH, Hiatt EE III, Kittle B (2005) Seed maturity, germination, and endophyte relationships in tall fescue. Crop Sci 45:859–863

    Article  Google Scholar 

  24. Insausti P, Chaneton EJ, Soriano A (1999) Flooding reverted grazing effects on plant community structure in mesocosms of lowland grassland. Oikos 84:266–276

    Article  Google Scholar 

  25. Jackson MB, Colmer TD (2005) Response and Adaptation by Plants to Flooding Stress. Ann Bot 96:501–505

    Article  PubMed  CAS  Google Scholar 

  26. Jensen AMD, Roulund N (2004) Occurrence of Neotyphodium endophytes in permanent grassland with perennial ryegrass (Lolium perenne) in Denmark. Agric Ecosyst Environ 104:419–427

    Article  Google Scholar 

  27. Koh S, Vicari M, Ball JP, Rakocevic T, Zaheer S, Hik DS, Bazely DR (2006) Rapid detection of fungal endophytes in grasses for large-scale studies. Funct Ecol 20:736–742

    Article  Google Scholar 

  28. Koh S, Hik DS (2007) Herbivory mediates grass–endophyte relationships. Ecology 88(11):2752–2757

    Article  PubMed  Google Scholar 

  29. Kover PX, Dolan TE, Clay K (1997) Potential versus realized transmission rates of a vertically and horizontally transmitted plant pathogen. Proc R Soc Lond B 264:903–909

    Article  Google Scholar 

  30. Lewis GC, Ravel C, Naffaa W, Astier C, Charmet G (1997) Occurrence of Acremonium endophytes in wild populations of Lolium spp in European countries and a relationship between level of infection and climate in France. Ann Appl Biol 130:227–238

    Article  Google Scholar 

  31. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassland Sci 52:1–14

    Article  Google Scholar 

  32. Moon CD, Scott B, Schardl CL, Christensen MJ (2000) Evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92:1103–1118

    Article  Google Scholar 

  33. Mueller-Dombois DR, Ellenberg H (1974) Aims and methods of vegetation ecology. Wiley, New York

    Google Scholar 

  34. Novas MV, Collantes M, Cabral D (2007) Environmental effects on grass-endophyte associations in the harsh conditions of south Patagonia. FEMS Microbiol Ecol 61:164–173

    Article  PubMed  CAS  Google Scholar 

  35. Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighboring plants. Funct Ecol 20:226–232

    Article  Google Scholar 

  36. Perelman SB, León RJC, Oesterheld M (2001) Cross-scale vegetation patterns of Flooding Pampa grasslands. J Ecol 89:562–577

    Article  Google Scholar 

  37. Ravel C, Michalakis Y, Chermet G (1997) The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 80:18–24

    Article  Google Scholar 

  38. Richardson DM, Allsopp N, D’Antonio C, Milton S, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  PubMed  CAS  Google Scholar 

  39. Rudgers JA, Brett Mattingly W, Koslow JM (2005) Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144:463–471

    Article  PubMed  Google Scholar 

  40. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  41. Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23(3):360–366

    Article  Google Scholar 

  42. Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapopulations. Proc R Soc Lond B 269:1397–1403

    Article  Google Scholar 

  43. Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90:569–578

    Article  Google Scholar 

  44. Siegel MR, Johnson MC, Varney DR, Nesmith WC, Buckner RC, Bush LP, Burrus PB II, Jones TA, Boiling JA (1984) A fungal endophyte in tall fescue: incidence and dissemination. Phytopathology 74(8):932–937

    Article  Google Scholar 

  45. Soreng RJ, Terrell EE (2003) /Schedonorus. In: Soreng RJ (ed) Catalogue of New World Grasses (Poaceae): IV. Subfamily Pooideae. Contributions from the United States National Herbarium, pp 605–607

  46. Soriano A, León RJC, Sala OE, Lavado RS, Deregibus VA, Cahuepé MA, Scaglia OA, Velázquez CA, Lemcoff JH (1991) Río de la Plata grasslands. In: Coupland RT (ed) Ecosystems of the world 8A, Natural grasslands. Introduction and western hemisphere. Elsevier, Netherlands, pp 367–407

    Google Scholar 

  47. Sugawara K, Inoue T, Yamashita M, Ohkubo H (2006) Distribution of the endophytic fungus, Neotyphodium occultans in naturalized Italian ryegrass in western Japan and its production of bioactive alkaloids known to repel insect pests. Grassland Sci 52:147–154

    Article  CAS  Google Scholar 

  48. Vila-Aiub MM, Martínez-Ghersa MA, Ghersa CM (2003) Evolution of herbicide resistance in weeds: vertically transmitted fungal endophytes as genetic entities. Evol Ecol 17:441–456

    Article  Google Scholar 

  49. Welty RE, Azevedo MD, Cooper TM (1987) Influence of moisture content, temperature, and length of storage on seed germination and survival of endophytic fungi in seeds of tall fescue and perennial ryegrass. Phytopathology 77:893–900

    Article  Google Scholar 

  50. Williams R, Bartholomew P (2005) Factors affecting Italian ryegrass (Lolium multiflorum L.) seed distribution. In: Murphy JJ (ed) Utilization of grazed grass in temperate animal systems. Wageningen, Netherlands, p 248

    Google Scholar 

Download references

Acknowledgments

We thank the Bordeu family for kindly permitting us to work on their property. We are also very grateful to M. M. Rabadán and M. Gundel for their technical assistance in the evaluation of endophyte presence, to P. Roset and S. Burkart for their helpful comments and to Rolando J.C. Leon for the transmission of his acknowledge upon the Pampean landscape. P.E.G., P.M.T. and L.A.G. hold a Research Scholarship from the National Research Council, Argentina. This study was supported by UBACYT G042 grant. Finally, the manuscript was significantly improved by the input from three anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pedro E. Gundel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gundel, P.E., Garibaldi, L.A., Tognetti, P.M. et al. Imperfect Vertical Transmission of the Endophyte Neotyphodium in Exotic Grasses in Grasslands of the Flooding Pampa. Microb Ecol 57, 740–748 (2009). https://doi.org/10.1007/s00248-008-9447-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-008-9447-y

Keywords

Navigation