Abstract
The incidence of epichloid endophytes in populations of wild grasses is usually variable, and the knowledge about distribution patterns and how environmental factors affect such an incidence is limited. Here we performed a broad scale survey data to study whether the distribution patterns and the incidence of vertically-transmitted endophytes in populations of two native grasses from South-America, Poa lanuginosa Poir. and Poa bonariensis (Lam.) Kunth., are associated with environmental characteristics. We also characterized the endophytes from different populations to establish if the genotype of the endophytes is also correlated with environmental variables. The incidence of endophytes ranged from 0 to 100 % in both host species. In P. lanuginosa, endophytes were only found in populations on sandy coastal dunes and their incidence was positively associated with winter regime rainfall and soil water availability in the growing season. In P. bonariensis, endophytes were only found in populations in xerophytic forests and their incidence was highly associated with plant community. The distributions of infested populations suggested that the endophytes are not found in those areas with the most favorable or most stressing growth conditions accordingly to climatic or edaphical characteristics. Only the vertically transmitted hybrid endophyte species Neotyphodium tembladerae was detected in both host species. Under the hypothesis of vertical transmission, these results suggested that the endophyte should have been lost in endophyte free populations but is maintained in populations established in environments presenting moderate stress as salinity or short drought periods.
Similar content being viewed by others
References
Afkhami ME, Rudgers JA (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am Nat 172:405–416
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 30:367–374
Cabrera AL (1976) Regiones fitogeográficas argentinas. In: Kugler WF (ed) Enciclopedia Argentina de agricultura y jardinería, Tomo 2, 2nd edn. Acme, Buenos Aires, pp 1–85
Cheplick GP (2004) Recovery from drought stress in Lolium perenne (Poaceae). Are fungal endophytes detrimental? Am J Bot 91:1960–1968
Christensen MJ, Saulsbury K, Simpson WR (2012) Conspicuous epiphytic growth of an interspecific hybrid Neotyphodium sp. endophyte on distorted host inflorescences. Fungal Biol 116:42–48
Chung K-R, Schardl CL (1997) Vegetative compatibility between and within Epichloë species. Mycologia 89:558–565
Clark EM, White JF Jr, 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 Methods 1:149–155
Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S099–S127
Crisci JV, Lopez Armengol MF (1983) Introducción a la Teoría y Práctica de la Taxonomía Numérica, Serie de Biología: Monografía no. 26. OEA, Washington DC
De Fina AL (1992) Aptitud agroclimática de la República Argentina. Academia Nacional de Agronomía y. Veterinaria, Buenos Aires
Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7:304–307
Faeth SH, Hayes CJ, Gardner DR (2010) Asexual endophytes in a native grass: tradeoffs in mortality, growth, reproduction, and alkaloid production. Microb Ecol 60:496–504
Gentile A, Rossi MS, Cabral D, Craven KD, Schardl CL (2005) Origin, divergence and phylogeny of epichloë endophytes of native Argentine grasses. Mol Phylogenet Evol 35:196–208
Giussani LM (2000) Phenetic similarity of dioecious species of Poa from Argentina and neighboring countries. Ann Mo Bot Gard 83:203–233
Giussani LM, Negritto MA, Romanutti A, Anton A, Soreng RJ (2012) Poa. In: Zuloaga FO, Rúgolo de Agrasar ZE, Anton AM (eds). Flora vascular de la República Argentina, Gráficamente Ediciones, Córdoba, pp 284339
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 30:422–430
Gundel PE, Batista WE, 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 Roy Soc B 275:897–905
Gundel PE, Zabalgogeazcoa I, Vázquez de Aldana BR (2011a) Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra). Crop Pasture Sci 62:1010–1016
Gundel PE, Garibaldi LA, Martínez-Ghersa MA, Ghersa CM (2011b) Neotyphodium endophyte transmission to Lolium multiflorum seeds depends on the host plant fitness. Environ Exp Bot 71:359–366
Hamilton CE, Faeth SH, Dowling TE (2009) Distribution of hybrid fungal symbionts and environmental stress. Microb Ecol 58:408–413
Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58:407–415
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 101:336–347
Iannone LJ, White JF Jr, Giussani LM, Cabral D, Novas MV (2011) Diversity and distribution of Neotyphodium-infected grasses in Argentina. Mycol Prog 10:9–19
Iannone LJ, Pinget AD, Nagabhyru P, De Battista JP, Schardl CL (2012a) Beneficial effects of Neotyphodium tembladerae and Neotyphodium pampeanum on a wild forage grass. Grass Forage Sci 67:382–390
Iannone LJ, Novas MV, Young CA, De Battista JP, Schardl CL (2012b) Endophytes of native grasses from South America: diversity and ecology. Fungal Ecol 5:357–363
Jackson ML (1982) Análisis químico de los suelos. Omega, Barcelona
Latch GCM, Christensen MJ (1985) Artificial infections of grasses with endophytes. Ann Appl Biol 107:17–24
Lembicz M, Górzyńska K, Olejniczak P, Leuchtmann A (2011) Geographical distribution and effects of choke disease caused by Epichloë typhina in populations of the grass Puccinellia distans in Poland. Sydowia 63:35–48
Lewis GC, Ravel C, Naffaa W, Astier C, Charmet G (1997) Ocurrence 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
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
Matteucci SD, Colma A (1982) Metodología para el estudio de la vegetación, Serie de Biología: Monografía no. 22. OEA, Washington DC
McCune B (1991) Multivariate analysis on the PC-ORD system. Oregon State University, Corvallis
Moy M, Belanger F, Duncan R, Freehoff A, Leary C, Meyer W, Sullivan R, White JF Jr (2000) Identification of epiphyllous mycelia nets on leaves of grasses infected by clavicipitaceous endophytes. Symbiosis 28:291–302
Nixon KC (1999) Winclada (Beta) Ver. 0.9.9 published by the author, Ithaca, New York. (http://www.cladistics.com/about_winc.htm)
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
Parodi L (1940) La distribución geográfica de los talares en la provincia de Buenos Aires. Darwiniana 4:33–57
Petrini O (1986) Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, van den Huevel J (eds) Microbiology of the phyllosphere, 1st edn. Cambridge University Press, Cambridge, pp 175–187
Ravel C, Michalakis Y, Charmet G (1997) The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 80:18–24
Ribichich AM (2002) El modelo clásico de la fitogeografía de Argentina. Un análisis crítico. Interciencia 27:669–675
Ribichich AM, Protomastro J (1998) Woody vegetation structure of xeric forest stands under different edaphic site conditions and disturbance histories in the Biosphere Reserve ‘Parque Costero del Sur’, Argentina. Plant Ecol 139:189–201
Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Rudgers JA, Afkhami ME, Rua MA, Davitt AJ, Hammer S, Huguet VM (2009) A fungus among us: Broad patterns of endophyte distribution in the grasses. Ecology 90:1531–1539
Saikkonen K, Alholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23:360–366
Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapopulations. Proc Roy Soc B 269:1397–1403
Schardl CL (1996) Epichloë species: fungal symbionts of grasses. Annu Rev Phytopathol 34:109–130
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340
Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90:569–578
Soriano A (1991) Río de la Plata grasslands. In: Coupland RT (ed) Ecosystems of the world 8A. Natural grasslands. Introduction and Western Hemisphere. Elsevier, Amsterdam, pp 367–407
Tadych M, Ambrose KV, Bergen MS, Belanger FC, White JF Jr (2012) Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers 54:117–131
Thornthwaite GW (1948) An approach to a rational classification of climate. Geogr Rev 38:59–64
Van der Maarel E (1981) Fluctuations in a coastal dune grassland due to fluctuations in rainfall: experimental evidence. Vegetatio 47:259–265
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 53:20–29
White JF Jr, Morgan Jones G, Morrow AC (1993) Taxonomy, life cycle, reproduction and detection of Acremonium endophytes. Agr Ecosyst Environ 44:13–37
White JF Jr, Martin TI, Cabral D (1996) Endophyte-host associations in forage grasses. XXIII. Conidia formation by Acremonium endophytes in the phylloplanes of Agrostis hiemalis and Poa rigidifolia. Mycologia 88:174–178
White JF Jr, 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 31:241–257
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 61:71–76
Acknowledgements
This research was supported by University of Buenos Aires (UBACyT 20020090300118), CONICET (PIP 1482), and ANPCyT, PAE-PICT Nº58. Support to CLS was from USDA-ARS Specific Cooperative Agreement grant 200911131030. This research was started under the supervision of Dr. Daniel Cabral.
PROPLAME-PRHIDEB-CONICET. Publication 193.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Iannone, L.J., Mc Cargo, P.D., Giussani, L.M. et al. Geographic distribution patterns of vertically transmitted endophytes in two native grasses in Argentina. Symbiosis 59, 99–110 (2013). https://doi.org/10.1007/s13199-012-0214-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-012-0214-y