Advertisement

Mycological Progress

, Volume 10, Issue 1, pp 9–19 | Cite as

Diversity and distribution of Neotyphodium-infected grasses in Argentina

  • Leopoldo J. IannoneEmail author
  • James F. WhiteJr.
  • Liliana M. Giussani
  • Daniel Cabral
  • María Victoria Novas
Original article

Abstract

In the present work, we studied the presence of “epichloë/neotyphodium endophytes” in native grasses from Argentina. An extensive area of this country, representative of several different environments, was studied. Nine new host species of the genera Briza, Bromus and Poa were observed to be infected with asexual seed-borne endophytes. Epichloë stromata were not observed on any grass species. The incidence of infection in natural populations was highly variable among host species and among populations of the same host species. Morphological characterization revealed differences among the endophytes of different host species and among endophytes of different populations of the same host species. We also summarize the previous knowledge and present unpublished data on host diversity and distribution of these fungi in Argentina. Our results are discussed and compared with previous studies on endophytes in Argentina. This work supports the hypothesis that sexual species (Epichloë) are not present in the southern hemisphere, and suggests the existence of a high diversity of asexual endophytes in South America.

Keywords

Neotyphodium Endophytes Diversity South America 

Notes

Acknowledgements

This paper is dedicated to the memory of Dr. Daniel Cabral, our friend, teacher and colleague, and one of the first scientists to perceive the biological relevance of these grass-fungus interactions in South America. This research was supported by University of Buenos Aires (UBACyT X833), CONICET (PIP5311, PIP 1482), and ANPCyT, PAE-PICT N°58. PRHIDEB-CONICET : Publication 179

References

  1. Afkhami ME, Rudgers JA (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am Nat 172:405–416PubMedCrossRefGoogle Scholar
  2. Bacon CW (1995) Toxic endophyte-infected tall fescue and range grasses: historic perspectives. J Anim Sci 73:861–870PubMedGoogle Scholar
  3. Bazely RD, Ball JP, Vicari M, tanentzap AJ, Bérenger M, Rakocevic T, Kok S (2007) Broad-scale patterns in the distribution of vertically transmitted, asexual endophytes in four naturally-occurring grasses in Sweden. Ecography 30:367–374CrossRefGoogle Scholar
  4. Bertoni MD, Cabral D, Romero N, Dubcovsky J (1993) Endofitos fúngicos en especies sudamericanas de Festuca (Poaceae). Bol Soc Argent Bot 29:25–34Google Scholar
  5. Burkart A (1969) Gramíneas: la familia de los pastos. Parte II. In: Flora Ilustrada de Entre Ríos (Argentina). INTA, Buenos AiresGoogle Scholar
  6. Cabral D, Cafaro MJ, Saidman B, Lugo M, Reddy PV, White JF Jr (1999) Evidence supporting the ocurrence of a new species of endophyte in some South American grasses. Mycologia 91:315–325CrossRefGoogle Scholar
  7. Cabrera AL (1970) Gramíneas. In: Flora de la Provincia de Buenos Aires. Parte II. INTA Buenos AiresGoogle Scholar
  8. Cabrera AL (1976) Regiones fitogeográficas argentinas. In: Kugler WF (ed) Enciclopedia Argentina de agricultura y jardinería. Tomo 2, 2nd edn. Acme, Buenos Aires, pp 1–85Google Scholar
  9. Chung KR, Schardl CL (1997) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycol Res 101:295–301CrossRefGoogle Scholar
  10. Clark EM, White JF, Patterson RM (1983) Improved histochemical techniques for the detection of Acremonium coenophialum in tall fescue and methods of in vitro culture of the fungus. J Microbiol Methh 1:149–155CrossRefGoogle Scholar
  11. Clarke BB, White JF, Hurley RH, Torres MS, Sun S, Huff DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis 90:994–998CrossRefGoogle Scholar
  12. Clay K (1990) Fungal endophyte of grasses. Annu Rev Ecol Syst 21:275–297CrossRefGoogle Scholar
  13. Clay K, Leuchtmann A (1989) Infection of woodland grasses by fungal endophytes. Mycologia 81:805–811CrossRefGoogle Scholar
  14. Colabelli M, Torres MS, Clausen AM, Fernandez ON, Peretti A (2007) Neotyphodium spp.—grass association in natural grassland in Argentina. In Proceedings of the 6th International symposium on Fungal Endophytes of Grasses, pp 95–99Google Scholar
  15. Fernandez OA, Busso CA (1997) Arid and semi-arid rangelands: two thirds of Argentina. RALA Report 200:41–60Google Scholar
  16. Fletcher LR, Harvey IC (1981) An association of a Lolium endophyte with ryegrass staggers. N Z Vet J 29:185–186PubMedGoogle Scholar
  17. Funk CR, White JF (1997) Use of natural and transformed endophytes for turf improvement. In: Bacon CW, Hill NS (eds) Neotyphodium/grass interactions. Plenum, New York, pp 229–239Google Scholar
  18. Gentile A, Rossi MA, Cabral D, Craven KD, Schardl CL (2005) Origin, divergence, and phylogeny of Epichloë endophytes of native Argentine grasses. Mol Phylogenet Evol 35:196–208PubMedCrossRefGoogle 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 30:422–430Google Scholar
  20. Gundel PE, Batista WB, Texeira M, Martinez-Ghersa MA, Omacini M, Ghersa CM (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and vertical transmission efficiency. Proc R Soc Lond B 275:897–905CrossRefGoogle Scholar
  21. Hill NS, Roach PK (2009) Endophyte survival during seed storage: endophyte—host interactions and heritability. Crop Sci 49:1425–1430CrossRefGoogle Scholar
  22. Iannone LJ, Cabral D (2006) Effects of the Neotyphodium endophyte status on plant performance of Bromus auleticus, a wild native grass from South America. Symbiosis 41:61–69CrossRefGoogle Scholar
  23. 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 101:336–347CrossRefGoogle Scholar
  24. Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71CrossRefGoogle Scholar
  25. Kuldau GA, Tsai HF, Scharld CL (1997) Molecular systematics of Clavicipitaceae supporting monophyly of genus Epichloë and for genus Ephelis. Mycologia 89:431–441CrossRefGoogle Scholar
  26. Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1(150–1):62Google Scholar
  27. Leyronas C, Raynal G (2001) Presence of Neotyphodium-like endophytes in European grasses. Ann Appl Biol 139:119–127CrossRefGoogle Scholar
  28. Lugo MA, Anton AM, Cabral D (1998) Micofilas en gramíneas Sudamericanas. An Jard Bot Madr 56:15–22CrossRefGoogle Scholar
  29. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  30. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassland Science 52:1–14CrossRefGoogle Scholar
  31. Millot JC (2001) Bromus auleticus: una nueva especie domesticada. In PROCISUR-IICA (ed) Diálogo LVI: los recursos fitogenéticos del género Bromus en el cono sur. Montevideo, pp 3–5Google Scholar
  32. Mirlohi A, Sabzalian MR, Sharifnabi B, Nekoui MK (2006) Widespread occurrence of Neotyphodium-like endophyte in populations of Bromus tomentellus Boiss.in Iran. FEMS Microbiol Lett 256(1):126–131PubMedCrossRefGoogle Scholar
  33. 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 94:694–711PubMedCrossRefGoogle Scholar
  34. Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13:1455–1467PubMedCrossRefGoogle Scholar
  35. Moon CD, Guillaumin J-J, Ravel C, Li C, Craven KD, Schardl CL (2007) New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae. Mycologia 99:895–905PubMedCrossRefGoogle Scholar
  36. Nicora EG (1978) Graminea. Parte III. In: Flora Patagónica. INTA, Buenos AiresGoogle Scholar
  37. Novas MV, Gentile A, Cabral D (2003) Comparative study of growth parameters on diaspores and seedlings between populations of Bromus setifolius from Patagonia, differing in Neotyphodium endophyte infection. Flora 198:421–426Google Scholar
  38. Novas MV, Collantes M, Cabral D (2007) Environmental effects on grass-endophyte associations in the harsh conditions of south Patagonia. FEMS Microbiol Ecol 61:164–173PubMedCrossRefGoogle Scholar
  39. Novas MV, Iannone LJ, Godeas A, Cabral D (2009) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog 8:75–81CrossRefGoogle Scholar
  40. Parodi LR (1950) Las gramíneas tóxicas para el ganado en la República Argentina. Rev Arg Agronomia :163–229Google Scholar
  41. Rivas H, Zanolli M (1909) La tembladera. Enfermedad propia de los animales herbívoros de las regiones andinas. Rev Fac Agron Vet Plata 5:5–35Google Scholar
  42. Rudgers JA, Afkhami ME, Rúa MA, Davitt JA, Hammer SA, Huguet VM (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90:1531–1539PubMedCrossRefGoogle Scholar
  43. Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Neimeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23:360–366CrossRefGoogle Scholar
  44. Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapoplations. Proc R Soc Lond B 269:1397–1403CrossRefGoogle Scholar
  45. Sampson K (1933) The systemic infection of grasses by Epichloë typhina (Pers.) Tul. Trans Br Mycol Soc 18:30–47CrossRefGoogle Scholar
  46. Schardl CL (1996) Epichloë species: fungals symbionts of grasses. Phytopathology 34:109–130CrossRefGoogle Scholar
  47. Schardl CL, Leuchtmann A, Chung KR, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol Biol Evol 14:133–143Google Scholar
  48. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbiosis of grasses with seed-borne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedCrossRefGoogle Scholar
  49. Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90:569–578CrossRefGoogle Scholar
  50. Stebbins GL (1981) Chromosomes and evolution in the genus Bromus (Gramineae). Bot Jahrb Syst 102(1–4):359–379Google Scholar
  51. Vila Aiub MM, Demartin EB, Maseda P, Gundel PE, Ghersa CM (2001) Exploración de la presencia de hongos endofíticos em pastos de la Estepa Patagónica. Actas de la I Reunión Binacional de EcologíaGoogle Scholar
  52. Wei YK, Gao YB, Xu H, Su D, Zhang X, Wang YH, Lin F, Chen L, Nie LY, Ren AZ (2006) Occurrence of endophytes in grasses native to northern China. Grass Forage Sci 61:422–429CrossRefGoogle Scholar
  53. 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 77:893–900CrossRefGoogle Scholar
  54. White JF (1987) Widespread distribution of endophytes in the Poaceae. Plant Dis 71:340–342CrossRefGoogle Scholar
  55. White JF (1992) Endophyte-host associations in grasses. XVII. Ecological and physiological features characteriszing Epichloë typhina and some anamorphic varities in England. Mycologia 84:431–441CrossRefGoogle Scholar
  56. White JF, Baldwin NA (1992) A preliminary enumeration of grass endophytes in west central Europe grasslands. Sydowia 44:78–84Google Scholar
  57. White JF, Cole GT (1985) Endophyte-host associations in forage grasses. I. Distribution of fungal endophytes in some species of Lolium and Festuca. Mycologia 77:323–327CrossRefGoogle Scholar
  58. White JF, 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
  59. White JF, Sullivan RF, Balady GA, Gianfagna TJ, Yue Q, Meyer WA, Cabral D (2001) A fungal endosymbiont of the grass Bromus setifolius: distribution in some Andean populations, identification and examination of beneficial properties. Symbiosis 31:241–257Google Scholar
  60. Zuloaga FO, Nicora EG, Rúgolo de Agrazar ZE, Morrone O, Pensiero J, Cialdella AM (1994) Catálogo de la familia Poaceae en la República Argentina. Missouri Botanical GardenGoogle Scholar

Copyright information

© German Mycological Society and Springer 2010

Authors and Affiliations

  • Leopoldo J. Iannone
    • 1
    • 2
    Email author
  • James F. WhiteJr.
    • 3
  • Liliana M. Giussani
    • 4
  • Daniel Cabral
    • 1
  • María Victoria Novas
    • 1
  1. 1.Lab. de Micología, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos Aires & PROPLAME-PRHIDEB-CONICETBuenos AiresArgentina
  2. 2.Departamento de Ingeniería Química, Facultad de IngenieríaUniversidad de Buenos AiresBuenos AiresArgentina
  3. 3.Department of Plant Biology & PathologyRutgers UniversityNew BrunswickUSA
  4. 4.Instituto de Botánica Darwinion—CONICETBuenos AiresArgentina

Personalised recommendations