Abstract
A new Epichloë species distributed in Africa, Europe, North America and South America on host genera Bromus, Festuca, Lolium and Poa is described. Stromata, characteristic of the genus, frequently occurred on the reproductive tillers of Poa secunda subsp. juncifolia, but neither perithecia nor mature asci were observed. Conidiogenous cells and conidial characteristics were in the range of Epichloë typhina. Regions of the genes encoding β-tubulin (tub2) and translation elongation factor 1-α (tef1) were amplified and sequenced. Phylogenetic analyses of these sequences grouped the Poa secunda subsp. juncifolia endophyte into one group within a non-hybrid Epichloë species complex. On the basis of morphology, host range and evolutionary history we propose that this endophyte represents a new species of Epichloë. The name Epichloë poae is proposed for this endophyte. The infectivity of the conidia produced on plants was evaluated. In the first experiment, using conidia of Epichloë poae from leaves and endophyte-free seeds of Poa secunda subsp. juncifolia we show that when germinating seeds and developing seedlings of the plant were exposed to conidia, 28–57 % of seedlings became infected by the endophyte. The non-inoculated control plants showed no colonization by the endophyte. In the following spring after vernalization, colonized plants on flowering culms produced stromata with conidia. In the second experiment, using stromal conidia and the same procedure, 19–42 % of seedlings of Poa secunda subsp. juncifolia became colonized by the endophyte. Our results demonstrate that Epichloë poae may spread to uninfected grass hosts by conidia frequently formed on the surfaces of plant leaves as well as by conidia formed on stromata.
Similar content being viewed by others
References
Bacon CW, Hinton DM (1988) Ascosporic iterative germination in Epichloë typhina. Trans Br Mycol Soc 90:563–569
Bacon CW, Hinton DM (1991) Microcyclic conidiation cycles in Epichloë typhina. Mycologia 83:743–751
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 Press, Boca Raton, pp 47–56
Bacon CW, Lyons PC, Porter JK, Robbins JD (1986) Ergot toxicity from endophyte-infected grasses: a review. Agron J 78:106–116
Barkworth ME, Anderton LK, Capels KM, Long S, Piep MB (2007) Manual of grasses for North America. Utah State University Press, Logan
Bischoff JF, White JF Jr (2005) Evolutionary development of the Clavicipitaceae. In: Dighton J, White JF Jr, Oudemans P (eds) The fungal community: its organization and role in the ecosystem. Taylor and Francis, Boca Raton, pp 505–518
Bouton JH, Easton S (2005) Endophyte in forage cultivars. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses. Blackwell Publishing, Professional, Ames, pp 327–340
Bouton JH, Gates RN, Belesky DP, Owsley M (1993) Yield and persistence of tall fescue in the southeastern costal plain after removal of its endophyte. Agron J 85:52–55
Brem D, Leuchtmann A (1999) High prevalence of horizontal transmission of the fungal endophyte Epichloë sylvatica. Bull Geobot Inst ETH 65:3–12
Bultman TL, White JF Jr, Bowdish TI, Welch AM, Johnston J (1995) Mutualistic transfer of Epichloë spermatia by Phorbia flies. Mycologia 87:182–189
Bultman TL, White JF Jr, Bowdish TI, Welch AM (1998) A new kind of mutualism between fungi and insects. Mycol Res 102:235–238
Bultman TL, Aguilera A, Sullivan TJ (2012) Influence of fungal isolates infecting tall fescue on multitrophic interactions. Fungal Ecol 5:372–378
Christensen MJ, Voisey CR (2009) Tall fescue-endophyte symbiosis. In: Fribourg HA, Hannaway DB, West CP (eds) Tall fescue for the twenty-first century. Agronomy Monograph 53. ASA, CSSA, SSSA, Madison, pp 251–272
Christensen MJ, Ball OJP, Bennett R, Schardl CL (1997) Fungal and host genotype effects on compatibility and vascular colonization by Epichloë festucae. Mycol Res 101:493–501
Christensen MJ, Bennett RJ, Schmid J (2002) Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycol Res 106:93–106
Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93
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) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycol Res 101:295–301
Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297
Clay K (2009) Defensive mutualism and grass endophytes: still valid after all these years? In: White JF Jr, Torres M (eds) Defensive mutualism in symbiotic association. CRC Press – Taylor and Francis Group, Boca Raton, pp 9–20
Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Amer Nat 160:S99–S127
Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL (2001a) Hybrid fungal endophytes symbiotic with grass Lolium pratense. Sydowia 53:44–73
Craven KD, Hsiau PTW, Leuchtmann A, Hollin W, Schardl CL (2001b) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Ann Missouri Bot Gard 88:14–34
Crawford KM, Land JM, Rudgers JA (2010) Fungal endophytes of native grasses decrease insect herbivore preference and performance. Oecologia 164:431–444
Dombrowski JE, Baldwin JC, Azevedo MD, Banowetz GM (2006) A sensitive PCR-based assay to detect Neotyphodium fungi in seed and plant tissue of tall fescue and ryegrass species. Crop Sci 46:1064–1070
Duell RW (1985) The bluegrass. In: Heath ME, Barnes RF, Metcalfe DS (eds) Forages: the science of grassland agriculture, 4th edn. Iowa State University Press, Ames, pp 188–197
Dugan FM, Sitton JW, Sullivan RF, White JF Jr (2002) The Neotyphodium endophyte of barley (Hordeum brevisubulatum subsp. violaceum) grows and sporulates on leaf surfaces of the host. Symbiosis 32:147–159
Eckblad F-E, Torkelsen A-E (1989) Epichloë typhina in Norway. Opera Bot 100:51–57
Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98:25–36
Faeth SH (2009) Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. Amer Nat 173:554–565
Faeth SH, Saari S (2012) Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions. Fungal Ecol 5:364–371
Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Amer Nat 161:310–325
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
Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88:369–383
Gundel PE, Garibaldi LA, Martínez-Ghersa MA, Ghersa CM (2012) Trade-off between seed number and weight: influence of a grass-endophyte symbiosis. Basic Appl Ecol 13:32–39
Hamilton CE, Dowling TE, Faeth SH (2010) Hybridization in endophyte symbionts alters host response to moisture and nutrient treatments. Microb Ecol 59:768–775
Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Diversity (this volume), doi:10.1007/s13225-012-0158-9
Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entom 54:323–342
Hultén E (1968) Flora of Alaska and neighboring territories. Stanford University Press, Stanford
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, Novas MV, Young CA, De Battista JP, Schardl CL (2012) Endophytes of native grasses from South America: biodiversity and ecology. Fungal Ecol 5:357–363
Jani A, Faeth SH, Gardner DR (2010) Asexual endophytes and associated alkaloids alter community structure and increase herbivore abundances on a native grass. Ecol Lett 13:106–117
Ji YL, Zhan LH, Kang Y, Sun XH, Yu HS, Wang ZW (2009) A new stromata-producing Neotyphodium species symbiotic with clonal grass Calamagrostis epigeios (L.) Roth. grown in China. Mycologia 101:200–205
Kang Y, Ji YL, Zhu K, Wang H, Miao H, Wang ZW (2011) A new Epichloë species with interspecific hybrid origins from Poa pratensis ssp. pratensis in Liyang, China. Mycologia 103:1341–1350
Koponen H, Mäkelä K (1976) Phyllachora graminis, P. silvatica, Epichloë typhina and Acrospermum graminum on grasses in Finland. Karstenia 15:46–55
Lembicz M, Górzyńska K, Leuchtmann A (2010) Choke disease caused by Epichloë bromicola in the grass Agropyron repens in Poland. Plant Dis 94:1372
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
Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1:150–162
Leuchtmann A, Schardl CL (1998) Mating compatibility and phylogenetic relationships among two new species of Epichloë and other congeneric European species. Mycol Res 102:1169–1182
Leyronas C, Raynal G (2008) Role of fungal ascospores in the infection of orchardgrass (Dactylis glomerata) by Epichloë typhina agent of choke disease. J Plant Pathol 90:15–21
Li W, Ji YL, Yu HS, Wang ZW (2006) A new species of Epichloë symbiotic with Chinese grasses. Mycologia 98:560–570
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
McNeill J (2011) Important decisions of the Nomenclature Section of the XVIII International Botanical Congress, Melbourne, 18–22 July 2011. Botanical Electronic News, ISSN 1188-603X, 441; http://www.ou.edu/cas/botany-micro/ben/ben441.html
Meijer G, Leuchtmann A (1999) Multistrain infections of the grass Brachypodium sylvaticum by its fungal endophyte Epichloë sylvatica. New Phytol 141:355–368
Moon CD, Scott B, Schardl CL, Christensen MJ (2000) The evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92:1103–1118
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 94:694–711
Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13:1455–1467
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 99:895–905
Moy M, Belanger F, Duncan R, Freehoff A, Leary C, Meyer WR, Sullivan R, White JF Jr (2000) Identification of epiphyllous mycelial nets on leaves of grasses infected by clavicipitaceous endophytes. Symbiosis 28:291–302
Moy M, Li HM, Sullivan R, White JF Jr, Belanger FC (2002) Endophytic fungal β-1,6-glucanase expression in the infected host grass. Plant Physiol 130:1298–1308
Olejniczak P, Lembicz M (2007) Age-specific response of the grass Puccinellia distans to the presence of a fungal endophyte. Oecologia 152:485–494
Panaccione DG, Johnson RD, Wang J, Young CA, Damrongkool P, Scott B, Schardl CL (2001) Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc Natl Acad Sci U S A 98:12820–12825
Pasko L, Ericson PGP, Elzanowski A (2011) Phylogenetic utility and evolution of indels: a study in neognathous birds. Mol Phylogenet Evol 61:760–771
Rudgers JA, Clay K (2008) An invasive plant–fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840
Saikkonen K, Saari S, Helander M (2010a) Defensive mutualism between plants and endophytic fungi? Fungal Diversity 41:101–113
Saikkonen K, Wäli PR, Helander M (2010b) Genetic compatibility determines endophyte-grass combinations. PLoS One 5:e11395. doi:10.1371/journal.pone.0011395
Schardl CL (2010) The epichloae, symbionts of the grass subfamily Poöideae. Ann Missouri Bot Gard 97:646–665
Schardl CL, Leuchtmann A (1999) Three new species of Epichloë symbiotic with North American grasses. Mycologia 91:95–107
Schardl CL, Leuchtmann A, Tsai HF, 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, Epichloë typhina. Genetics 136:1307–1317
Schardl CL, Leuchtmann A, Chung K-R, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol Biol Evol 14:133–143
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grass with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340
Schardl CL, Scott B, Florea S, Zhang D (2009) Epichloë endophytes: Clavicipitaceous symbionts of grasses. In: Deising HB (ed) The Mycota V: plant relationships, 2nd edn. Springer, Berlin, pp 275–306
Schiestl FP, Steinebrunner F, Schulz C, von Reuß S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Lett 2:401–404
Selosse M-A, Schardl CL (2007) Fungal endophytes of grasses: hybrids rescued by vertical transmission? An evolutionary perspective. New Phytol 173:452–458
Siegel MR, Johnson MC, Varney DR, Nesmith WC, Buckner RC, Bush LP, Burrus PB II, Jones TA, Boling JA (1984) A fungal endophyte in tall fescue: incidence and dissemination. Phytopathology 74:932–937
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 9:369–381
Soreng RJ (1991) Notes on new infraspecific taxa and hybrids in North American Poa (Poaceae). Phytologia 71:390–413
Soreng RJ (2009) Poa L. In: Anderton LK, Barkworth ME (eds) Grasses of the intermountain region. Intermountain Herbarium, Utah State University, Logan, pp 108–135
Summerbell RC, Gueidan C, Schroers H-J, de Hoog GS, Starink M, Arocha Rosete Y, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68:139–162
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Tadych M, White JF Jr (2007) Ecology of epiphyllous stages of endophytes and implications for horizontal dissemination. In: Popay AJ, Thom ER (eds) Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. Grassland Research and Practice Series No. 13. New Zealand Grass Association, Christchurch, pp 157–161
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 111:466–472
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Torres MT, White JF Jr, Zhang X, Hinton DM, Bacon CW (2012) Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecol 5:322–330
Tsai H-F, Liu J-S, Staben C, Christensen MJ, Latch GCM, Siegel MR, Schardl CL (1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci U S A 91:2542–2546
Vali U, Brandstrom M, Johansson M, Ellegren H (2008) Insertion-deletion polymorphisms (indels) as genetic markers in natural populations. BMC Genet 9:8
Wäli PR, Ahlholm J, 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
Western JH, Cavett JJ (1959) The choke disease of cocksfoot (Dactylis glomerata) caused by Epichloë typhina (Fr.) Tul. Trans Br Mycol Soc 42:298–307
White JF Jr (1988) Endophyte-host associations in forage grasses XI. A proposal concerning origin and evolution. Mycologia 80:442–446
White JF Jr (1993) Structure and mating system of the graminicolous fungal epibiont Echinodothis tuberiformis (Clavicipitales). Am J Bot 80:1465–1471
White JF Jr, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plantarum 138:440–446
White JF Jr, Morrow AC, Morgan-Jones G, Chambless DA (1991) Endophyte-host associations in forage grasses. XIV. Primary stromata formation and seed transmission in Epichloë typhina: development and regulatory aspects. Mycologia 83:72–81
White JF Jr, Halisky PM, Sun SC, Morgan-Jones G, Funk CR Jr (1992) Endophyte-host associations in grasses. XVI. Patterns of endophyte distribution in species of the tribe Agrostideae. Am J Bot 79:472–477
White JF Jr, Martin TI, Cabral D (1996) Endophyte-host associations in grasses. XXII. Conidia formation by Acremonium endophytes on the phylloplanes of Agrostis hiemalis and Poa rigidifolia. Mycologia 88:174–178
White JF Jr, Belanger F, Meyer W, Sullivan RF, Bischoff JF, Lewis EA (2002) Clavicipitalean fungal epibionts and endophytes – development of symbiotic interactions with plants. Symbiosis 33:201–213
Zabalgogeazcoa I, Gaarcia Criado B, Bony S (2002) Identification of the fungal endophyte Epichloë festucae in the fine fescue Festuca ampla. Plant Dis 86:1272
Zabalgogeazcoa I, Garcia Ciudad A, Leuchtmann A, Vazquez de Aldana BR, Garcia Criado B (2008) Effects of choke disease in the grass Brachypodium phoenicoides. Plant Pathol 57:467–472
Zhang X, Ren A-Z, Wei Y-K, Lin F, Li C, Liu Z-J, Gao Y-B (2009) Taxonomy, diversity and origins of symbiotic endophytes of Achnatherum sibiricum in the Inner Mongolia steppe of China. FEMS Microbiol Lett 301:12–20
Acknowledgments
We are grateful to several reviewers for constructive suggestions that improved this manuscript. This research program was supported in part by the New Jersey Agricultural Experiment Station and the Rutgers Turfgrass Science Center.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tadych, M., Ambrose, K.V., Bergen, M.S. et al. Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Diversity 54, 117–131 (2012). https://doi.org/10.1007/s13225-012-0170-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13225-012-0170-0