Characterisation of novel perennial ryegrass host–Neotyphodium endophyte associations
P. Tian A B C D E , T.-N. Le A E , E. J. Ludlow A D E , K. F. Smith B C D E , J. W. Forster A C D E , K. M. Guthridge A D E and G. C. Spangenberg A C D E F
+ Author Affiliations
- Author Affiliations
A Department of Environment and Primary Industries, Biosciences Research Division, AgriBio, The Centre for AgriBioscience, 5 Ring Road, Bundoora, Vic. 3083, Australia.
B Department of Environment and Primary Industries, Biosciences Research Division, Hamilton Centre, Mount Napier Road, Hamilton, Vic. 3300, Australia.
C La Trobe University, Bundoora, Vic. 3083, Australia.
D Molecular Plant Breeding Cooperative Research Centre, Victorian AgriBiosciences Centre, La Trobe Research and Development Park, Bundoora, Vic. 3083, Australia.
E Dairy Futures Cooperative Research Centre, AgriBio, the Centre for AgriBioscience, 5 Ring Road, Bundoora, Vic. 3083, Australia.
F Corresponding author. Email: german.spangenberg@depi.vic.gov.au
Crop and Pasture Science 64(7) 716-725 https://doi.org/10.1071/CP13067
Submitted: 18 February 2013 Accepted: 12 August 2013 Published: 4 October 2013
Abstract
The temperate pasture grass Lolium perenne L. is commonly found in symbiotic association with the asexual fungal endophyte Neotyphodium lolii. Levels of endophyte colonisation and alkaloid content were evaluated in associations formed by plant genotypes from cv. Bronsyn with the standard endophyte (SE) and five distinct commercial endophyte strains. Bronsyn–SE produced all of the measured alkaloids (lolitrem B, peramine, and ergovaline). Bronsyn–AR1 produced only peramine, while Bronsyn–AR37 produced none of the tested alkaloids. Bronsyn–NEA2, Bronsyn–NEA3, and Bronsyn–NEA6 produced both ergovaline and peramine. Both endophyte strain and host genotype exerted significant effects on alkaloid production. Analysis of endophyte colonisation using qPCR revealed differences between each association. With the exception of Bronsyn–AR1 and Bronsyn–NEA3, host genotype also significantly affected colonisation levels. Phenotypic performance of each association was also assessed, based on measurement of morphological traits under glasshouse conditions in hydroponic culture. Significant variation due to different endophyte and host genotypes was observed. Collectively, these studies confirm that differences in both endophyte and host genotypes contribute to host–endophyte performance in a complex interactive manner.
Additional keywords: colonisation, ergovaline, lolitrem B, Lolium, morphogenesis, peramine, symbiosis.
References
Ball OJ-P, Prestidge RA, Sprosen JM (1995) Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Applied and Environmental Microbiology 61, 1527–1533.Belesky DP, Fedders JM (1995) Tall fescue development in response to Acremonium coenophialum and soil acidity. Crop Science 35, 529–533.
| Tall fescue development in response to Acremonium coenophialum and soil acidity.Crossref | GoogleScholarGoogle Scholar |
Belesky DP, Devine OJ, Pallas JE, Stringer WC (1987) Photosynthetic activity of tall fescue as influenced by a fungal endophyte. Photosynthetica 21, 82–87.
Belesky DP, Stringer WC, Plattner RD (1989) Influence of endophyte and water regime upon tall fescue accessions. II. Pyrrolizidine and ergopeptine alkaloids. Annals of Botany 64, 343–349.
Bluett SJ, Thom ER, Clark DA, Macdonald KA, Minneé EMK (2005a) Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato. New Zealand Journal of Agricultural Research 48, 197–212.
| Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato.Crossref | GoogleScholarGoogle Scholar |
Bluett SJ, Thom ER, Clark DA, Waugh CD (2005b) Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain. Australian Journal of Experimental Agriculture 45, 11–19.
| Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain.Crossref | GoogleScholarGoogle Scholar |
Bultman TL, McNeill MR, Goldson SL (2003) Isolate-dependent impacts of fungal endophytes in a multitrophic interaction. Oikos 102, 491–496.
| Isolate-dependent impacts of fungal endophytes in a multitrophic interaction.Crossref | GoogleScholarGoogle Scholar |
Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology 114, 1–7.
Cheplick GP (1997) Effects of endophytic fungi on the phenotypic plasticity of Lolium perenne (Poaceae). American Journal of Botany 84, 34–40.
| Effects of endophytic fungi on the phenotypic plasticity of Lolium perenne (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Cheplick GP (1998) Genotypic variation in the regrowth of Lolium perenne following clipping: effects of nutrients and endophytic fungi. Functional Ecology 12, 176–184.
| Genotypic variation in the regrowth of Lolium perenne following clipping: effects of nutrients and endophytic fungi.Crossref | GoogleScholarGoogle Scholar |
Christensen MJ (1995) Variation in the ability of Acremonium endophytes of Lolium perenne, Festuca arundinacea and F. pratensis to form compatible associations in the three grasses. Mycological Research 99, 466–470.
| Variation in the ability of Acremonium endophytes of Lolium perenne, Festuca arundinacea and F. pratensis to form compatible associations in the three grasses.Crossref | GoogleScholarGoogle Scholar |
Christensen MJ, Leuchtmann A, Rowan DD, Tapper BA (1993) Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial ryegrass (Lolium perenne). Mycological Research 97, 1083–1092.
| Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial ryegrass (Lolium perenne).Crossref | GoogleScholarGoogle Scholar |
Christensen MJ, Bennett RJ, Schmid J (2002) Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycological Research 106, 93–106.
| Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses.Crossref | GoogleScholarGoogle Scholar |
Clay K (1993) The ecology and evolution of endophytes. Agriculture, Ecosystems & Environment 44, 39–64.
| The ecology and evolution of endophytes.Crossref | GoogleScholarGoogle Scholar |
di Menna ME, Finch SC, Popay AJ, Smith BL (2012) A review of the Neotyphodium lolii/Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers. New Zealand Veterinary Journal 60, 315–328.
| A review of the Neotyphodium lolii/Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bgsVWjuw%3D%3D&md5=8651e0a89271d3b93ccf108c341b0e97CAS | 22913513PubMed |
Easton HS, Latch GCM, Tapper BA, Ball OJ-P (2002) Ryegrass host genetic control of contentrations of endophyte-derived alkaloids. Crop Science 42, 51–57.
| Ryegrass host genetic control of contentrations of endophyte-derived alkaloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVantb8%3D&md5=0567d52cf8eb0d3f51a3fc98939d37e4CAS | 11756253PubMed |
Faeth SH, Bultman TL (2002) Endophytic fungi and interactions among host plants, herbivores and natural enemies. In ‘Multitrophic level interactions’. (Eds T Tscharntke, BA Hawkins) pp. 89–123. (Cambridge University Press: Cambridge, UK)
Faeth SH, Sullivan TJ (2003) Mutualistic, asexual endophytes in a native grass are usually parasitic. American Naturalist 161, 310–325.
| Mutualistic, asexual endophytes in a native grass are usually parasitic.Crossref | GoogleScholarGoogle Scholar | 12675375PubMed |
Fleetwood DJ, Khan AK, Johnson RD, Young CA, Mittal S, Wrenn RE, Hesse U, Foster SJ, Schardl CL, Scott B (2011) Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses. Genome Biology and Evolution 3, 1253–1264.
| Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltF2mtL0%3D&md5=9aeae633fff0e4ed26a989188fec808fCAS | 21948396PubMed |
Fletcher LR, Easton HS (1997) The evaluation and use of endophytes for pasture improvement. In ‘Neotyphodium/grass interactions’. (Eds CW Bacon, NS Hill) pp. 209–227. (Plenum Press: New York)
Fletcher LR, Sutherland BL (2009) Sheep responses to grazing ryegrass with AR37 endophyte. Proceedings of the New Zealand Grassland Association 71, 127–133.
Gallagher RT, Hawkes AD, Stewart JM (1985) Rapid determination of the neurotoxin lolitrem B in perennial ryegrass by high-performance liquid chromatography with fluorescence detection. Journal of Chromatography. A 321, 217–226.
| Rapid determination of the neurotoxin lolitrem B in perennial ryegrass by high-performance liquid chromatography with fluorescence detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvF2js7Y%3D&md5=a2a22f6148a70ca077a9198a02c69298CAS |
Guthridge KM, Dupal MP, Kölliker R, Jones ES, Smith KF, Forster JW (2001) AFLP analysis of genetic diversity within and between populations of perennial ryegrass (Lolium perenne L.). Euphytica 122, 191–201.
| AFLP analysis of genetic diversity within and between populations of perennial ryegrass (Lolium perenne L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xltlahsg%3D%3D&md5=fd8a5f09115d1cafc25cc726c22b151cCAS |
Hahn H, McManus MT, Warnstorff K, Monahan BJ, Young CA, Davies E, Tapper BA, Scott B (2008) Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environmental and Experimental Botany 63, 183–199.
| Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit.Crossref | GoogleScholarGoogle Scholar |
Hayes BJ, Cogan NOI, Pembleton LW, Goddard ME, Wang J, Spangenberg GC, Forster JW (2013) Prospects for genomic selection in forage plant species. Plant Breeding 132, 133–143.
| Prospects for genomic selection in forage plant species.Crossref | GoogleScholarGoogle Scholar |
Hiatt EE, Hill NS (1997) Neotyphodium coenophialum mycelial protein and herbage mass effects on ergot alkaloid concentration in tall fescue. Journal of Chemical Ecology 23, 2721–2736.
| Neotyphodium coenophialum mycelial protein and herbage mass effects on ergot alkaloid concentration in tall fescue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtleksA%3D%3D&md5=62453655b6c8a0e32043299925c71350CAS |
Hume D, Ryan D, Cooper B, Popay A (2007) Agronomic performance of AR37-infected ryegrass in northern New Zealand. Proceedings of the New Zealand Grassland Association 69, 201–205.
Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. Journal of Applied Ecology 42, 762–769.
| Reduced herbivore resistance from a novel grass-endophyte association.Crossref | GoogleScholarGoogle Scholar |
Jung GA, Van Wijk AJP, Hunt WF, Watson CE (1996) Ryegrasses. In ‘Cool-season forage grasses’. (Eds LE Moser, DR Buxton, MD Casler) pp. 605–641. (ASA, CSSA and SSSA: Madison, WI)
Justus M, Witte L, Hartmann T (1997) Levels and tissue distribution of loline alkaloids in endophyte-infected Festuca pratensis. Phytochemistry 44, 51–57.
| Levels and tissue distribution of loline alkaloids in endophyte-infected Festuca pratensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtl2ntQ%3D%3D&md5=9cc39f6aa0b794b6815dae84f7012444CAS |
Kaur J, Ekanayake PN, Rabinovich M, Ludlow EJ, Tian P, Rochfort SJ, Guthridge KM, Forster JW, Spangenberg GC (2012) Analysis of compatibility and stability in designer endophyte-grass associations between perennial ryegrass and Neotyphodium species. In ‘Proceedings of the 7th International Symposium on the Molecular Breeding of Forage and Turf 2012’. Salt Lake City, UT. (Eds BS Bushman, GC Spangenberg) p. 73. (MBFT Organizing Committee)
Keogh RG, Tapper BA, Fletcher RH (1996) Distributions of the fungal endophyte Acremonium lolii, and of the alkaloids lolitrem B and peramine, within perennial ryegrass. New Zealand Journal of Agricultural Research 39, 121–127.
| Distributions of the fungal endophyte Acremonium lolii, and of the alkaloids lolitrem B and peramine, within perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvVegt7k%3D&md5=d6a6a9eac1d6fc6d1735c744fb5ecd9bCAS |
Lane GA, Ball OJ-P, Davies E, Davidson C (1997) Ergovaline distribution in perennial ryegrass naturally infected with endophyte. In ‘Neotyphodium/grass interactions’. (Eds CW Bacon, NS Hill) pp. 65–67. (Plenum Press: New York)
Latch GCM (1994) Influence of Acremonium endophytes on perennial grass improvement. New Zealand Journal of Agricultural Research 37, 311–318.
| Influence of Acremonium endophytes on perennial grass improvement.Crossref | GoogleScholarGoogle Scholar |
Latch GCM, Christensen MJ, Samuels GJ (1984) Five endophytes of Lolium and Festuca in New Zealand. Mycotaxon 20, 535–550.
Lean IJ (2001) Association between feeding perennial ryegrass (Lolium perenne cultivar Grasslands Impact) containing high concentrations of ergovaline, and health and productivity in a herd of lactating dairy cows. Australian Veterinary Journal 79, 262–264.
| Association between feeding perennial ryegrass (Lolium perenne cultivar Grasslands Impact) containing high concentrations of ergovaline, and health and productivity in a herd of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlGqtLo%3D&md5=73eb943795c06aefec11c9309ce418faCAS | 11349413PubMed |
Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytologist 133, 727–733.
| Physiological responses of Festuca arundinacea to fungal endophyte infection.Crossref | GoogleScholarGoogle Scholar |
Marks S, Clay K, Cheplick GP (1991) Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. Journal of Applied Ecology 28, 194–204.
| Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne.Crossref | GoogleScholarGoogle Scholar |
Moate PJ, Williams SRO, Grainger C, Hannah MC, Mapleson D, Auldist MJ, Greenwood JS, Popay AJ, Hume DE, Mace WJ, Wales WJ (2012) Effects of wild-type, AR1 and AR37 endophyte-infected perennial ryegrass on dairy production in Victoria, Australia. Animal Production Science 52, 1117–1130.
| Effects of wild-type, AR1 and AR37 endophyte-infected perennial ryegrass on dairy production in Victoria, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Wju7zL&md5=c61e7861d39bcded463ddfafc849c358CAS |
Musgrave DR (1984) Detection of an endophytic fungus of Lolium perenne using enzyme-linked immunosorbent assay (ELISA). New Zealand Journal of Agricultural Research 27, 283–288.
| Detection of an endophytic fungus of Lolium perenne using enzyme-linked immunosorbent assay (ELISA).Crossref | GoogleScholarGoogle Scholar |
Paterson J, Forcherio C, Larson B, Samford M, Kerley M (1995) The effects of fescue toxicosis on beef cattle productivity. Journal of Animal Science 73, 889–898.
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Pennell CGL, Popay AJ, Ball OJP, Hume DE, Baird DB (2005) Occurrence and impact of pasture mealybug (Balanococcus poae) and root aphid (Aploneura lentisci) on ryegrass (Lolium spp.) with and without infection by Neotyphodium fungal endophytes. New Zealand Journal of Agricultural Research 48, 329–337.
| Occurrence and impact of pasture mealybug (Balanococcus poae) and root aphid (Aploneura lentisci) on ryegrass (Lolium spp.) with and without infection by Neotyphodium fungal endophytes.Crossref | GoogleScholarGoogle Scholar |
Popay AJ, Baltus JG (2001) Black beetle damage to perennial ryegrass infected with AR1 endophyte. Proceedings of the New Zealand Grassland Association 63, 267–271.
Popay AJ, Hume DE (2011) Endophytes improve ryegrass persistence by controlling insects. In ‘Pasture Persistence Symposium’. Grassland Research and Practice Series No. 15. (Ed. CF Mercer) pp. 149–156. (New Zealand Grassland Association: Dunedin, New Zealand)
Popay AJ, Hume DE, Davis KL, Tapper BA (2003) Interactions between endophyte (Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil (Listronotus bonariensis). New Zealand Journal of Agricultural Research 46, 311–319.
| Interactions between endophyte (Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil (Listronotus bonariensis).Crossref | GoogleScholarGoogle Scholar |
Porter JK (1995) Analysis of endophyte toxins: fescue and other grasses toxic to livestock. Journal of Animal Science 73, 871–880.
Prestidge RA (1993) Causes and control of perennial ryegrass staggers in New Zealand. Agriculture, Ecosystems & Environment 44, 283–300.
| Causes and control of perennial ryegrass staggers in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist 173, 787–797.
| High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGgsbg%3D&md5=5cef6fd4691179bfd5257af2dc9e5d17CAS | 17286827PubMed |
Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiology 146, 1440–1453.
| Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVKgur8%3D&md5=0aadfe9c3dfe57f0e94e1e62713b2f6aCAS | 18218971PubMed |
Rasmussen S, Parsons A, Newman JA (2009) Metabolomics analysis of the Lolium perenne–Neotyphodium lolii symbiosis: more than just alkaloids? Phytochemistry Reviews 8, 535–550.
| Metabolomics analysis of the Lolium perenne–Neotyphodium lolii symbiosis: more than just alkaloids?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Cqur3K&md5=24f7a401763c8adf9da2c0a1c0db41e7CAS |
Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends in Plant Science 9, 275–280.
| Evolution of endophyte–plant symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVemtbY%3D&md5=4673efb48a0e6697b9573e819a3a6bf9CAS | 15165558PubMed |
Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O’Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, Leistner E, Leuchtmann A, Li C, Liu J, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z (2013) Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLOS Genetics 9, e1003323
| Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlSksr0%3D&md5=22f77e18e339d742d8313823b948f7dbCAS | 23468653PubMed |
Schmidt D, Christensen MJ (1999) Ryegrass endophyte: host/fungus interaction. In ‘Ryegrass–endophyte: An essential New Zealand symbiosis’. Grassland Research and Practice Series No. 7. (Eds D Woodfield, HS Easton) pp. 101–106. (New Zealand Grassland Association: Napier, New Zealand)
Schmidt SP, Osborn TG (1993) Effects of endophyte-infected tall fescue on animal performance. Agriculture, Ecosystems & Environment 44, 233–262.
| Effects of endophyte-infected tall fescue on animal performance.Crossref | GoogleScholarGoogle Scholar |
Siegel MR, Latch GC, Johnson MC (1987) Fungal endophytes of grasses. Annual Review of Phytopathology 25, 293–315.
| Fungal endophytes of grasses.Crossref | GoogleScholarGoogle Scholar |
Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990) Fungal endophyte-infected grasses: Alkaloid accumulation and aphid responses. Journal of Chemical Ecology 16, 3301–3315.
| Fungal endophyte-infected grasses: Alkaloid accumulation and aphid responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpvVCruw%3D%3D&md5=82701b5584ab77aa17987786e7b46801CAS |
Spiering MJ, Lane GA, Christensen MJ, Schmid J (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66, 195–202.
| Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVektw%3D%3D&md5=f5b5fd2e099c1a37930d33306383cc4cCAS | 15652576PubMed |
Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, Schmid J (2001) In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Applied and Environmental Microbiology 67, 5377–5383.
| In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFehs7Y%3D&md5=b796b87fd5d3716c8794db3a506a148cCAS | 11722882PubMed |
Tapper BA, Lane GA (2004) Janthitrems found in a Neotyphodium endophyte of perennial ryegrass. In ‘5th International Symposium on Neotyphodium/Grass Interactions’. Fayetteville, AR. (Eds R Kallenbach, CJ Rosenkrans, TR Lock) pp. 301. (University of Arkansas Press: Fayetteville, AR)
Thom ER, Popay AJ, Hume DE, Fletcher LR (2012) Evaluating the performance of endophytes in farm systems to improve farmer outcomes—a review. Crop & Pasture Science 63, 927–943.
| Evaluating the performance of endophytes in farm systems to improve farmer outcomes—a review.Crossref | GoogleScholarGoogle Scholar |
Tian P, Le T-N, Smith KF, Forster JW, Guthridge KM, Spangenberg GC (2013) Stability and viability of novel perennial ryegrass host–Neotyphodium endophyte associations. Crop & Pasture Science 64, 39–50.
| Stability and viability of novel perennial ryegrass host–Neotyphodium endophyte associations.Crossref | GoogleScholarGoogle Scholar |
Tor-Agbidye J, Blythe LL, Craig AM (2001) Correlation of endophyte toxins (ergovaline and lolitrem B) with clinical disease: fescue foot and perennial ryegrass staggers. Veterinary and Human Toxicology 43, 140–146.
van Zijll de Jong E, Dobrowolski MP, Bannan NIR, Stewart AV, Smith KF, Spangenberg GC, Forster JW (2008a) Global genetic diversity of the perennial ryegrass fungal endophyte Neotyphodium lolii. Crop Science 48, 1487–1501.
| Global genetic diversity of the perennial ryegrass fungal endophyte Neotyphodium lolii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslajsrw%3D&md5=7b461d9b350de27fbaa58f4983ca38a6CAS |
van Zijll de Jong E, Dobrowolski MP, Sandford A, Smith KF, Willocks MJ, Spangenberg GC, Forster JW (2008b) Detection and characterisation of novel fungal endophyte genotypic variation in cultivars of perennial ryegrass (Lolium perenne L.). Australian Journal of Agricultural Research 59, 214–221.
| Detection and characterisation of novel fungal endophyte genotypic variation in cultivars of perennial ryegrass (Lolium perenne L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVKjtLo%3D&md5=f02f8e96f72c5d15497b479425a00f5dCAS |
Wang J, Dobrowolski MP, Cogan NOI, Forster JW, Smith KF (2009) Assignment of individual genotypes to specific forage cultivars of perennial ryegrass based on SSR markers. Crop Science 49, 49–58.
| Assignment of individual genotypes to specific forage cultivars of perennial ryegrass based on SSR markers.Crossref | GoogleScholarGoogle Scholar |
Young C, Bryant M, Christensen M, Tapper B, Bryan G, Scott B (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Molecular Genetics and Genomics 274, 13–29.
| Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGntrrF&md5=680aa2bbbd50c38118b8e2ffeba191ecCAS | 15991026PubMed |
Young CA, Tapper BA, May K, Moon CD, Schardl CL, Scott B (2009) Indole-diterpene biosynthetic capability of Epichloë endophytes as predicted by ltm gene analysis. Applied and Environmental Microbiology 75, 2200–2211.
| Indole-diterpene biosynthetic capability of Epichloë endophytes as predicted by ltm gene analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksFWltbw%3D&md5=89c63e0fe30025224d63b51070528161CAS | 19181837PubMed |
