Epichloë Endophyte Infection Rates and Alkaloid Content in Commercially Available Grass Seed Mixtures in Europe
Abstract
:1. Introduction
2. Materials and Methods
2.1. Seed Sampling
2.2. Endophyte Detection by Multiplex PCR
2.3. Alkaloid Analyses
3. Results
4. Discussion
- (1)
- When establishing pastures for grazing animals, we suggest avoiding Epichloë infected seed mixtures, especially with regard to seed mixtures containing perennial ryegrass varieties.
- (2)
- Seed companies could conduct regular tests on Epichloë infections of the breeding and seed material and provide detailed information on the exact composition and Epichloë infection of the seed mixtures to consumers.
- (3)
- The use of Epichloë strains incapable of producing the vertebrate toxic compounds lolitrem B and ergovaline could be utilized in European perennial ryegrass breeding, with simultaneous testing the risk of toxicosis.
- (4)
- Finally, we would like to call for attention in the EU and other European states to promote research on the neglected risks of intoxications by Epichloë infected host grasses on European grasslands.
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Franco, C.; Michelsen, P.; Percy, N.; Conn, V.; Listiana, E.; Moll, S.; Loria, R.; Coombs, J. Actinobacterial endophytes for improved crop performance. Australas. Plant Pathol. 2007, 36, 524–531. [Google Scholar] [CrossRef]
- Vujanovic, V.; Germida, J.J. Seed endosymbiosis: A vital relationship in providing prenatal care to plants. Can. J. Plant Sci. 2017, 97, 972–981. [Google Scholar] [CrossRef] [Green Version]
- Gundel, P.E.; Pérez, L.I.; Helander, M.; Saikkonen, K. Symbiotically modified organisms: Nontoxic fungal endophytes in grasses. Trends Plant Sci. 2013, 18, 420–427. [Google Scholar] [CrossRef] [PubMed]
- Simpson, W.R.; Faville, M.J.; Moraga, R.A.; Williams, W.M.; Mcmanus, M.T.; Johnson, R.D. Epichloë fungal endophytes and the formation of synthetic symbioses in Hordeeae (=Triticeae) grasses. J. Syst. Evol. 2014, 52, 794–806. [Google Scholar] [CrossRef]
- Song, Q.-Y.; Li, F.; Nan, Z.; Coulter, J.; Wei, W.-J. Do Epichloë endophytes and their grass symbiosis only produce toxic alkaloids to insects and livestock? J. Agric. Food Chem. 2020, 68, 1169–1185. [Google Scholar] [CrossRef]
- Spangenberg, G.; Wang, Z.-Y.; Potrykus, I. Biotechnology in Forage and Turf Grass Improvement; Springer Science & Business Media: Berlin/Heidelberg, Germany, 2012; ISBN 978-3-642-72051-2. [Google Scholar]
- Leuchtmann, A.; Bacon, C.W.; Schardl, C.L.; White, J.F.; Tadych, M. Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 2014, 106, 202–215. [Google Scholar] [CrossRef]
- Cheplick, G.P.; Faeth, S.H.; Faeth, S. Ecology and Evolution of the Grass-Endophyte Symbiosis; Oxford University Press: New York, NY, USA, 2009; ISBN 978-0-19-530808-2. [Google Scholar]
- Hume, D.E.; Ryan, G.D.; Gibert, A.; Helander, M.; Mirlohi, A.; Sabzalian, M.R. Epichloë fungal endophytes for grassland ecosystems. In Sustainable Agriculture Reviews: Volume 19; Lichtfouse, E., Ed.; Sustainable Agriculture Reviews; Springer International Publishing: Cham, Switzerland, 2016; pp. 233–305. ISBN 978-3-319-26777-7. [Google Scholar]
- Müller, C.B.; Krauss, J. Symbiosis between grasses and asexual fungal endophytes. Curr. Opin. Plant Biol. 2005, 8, 450–456. [Google Scholar] [CrossRef]
- Schardl, C.L.; Leuchtmann, A.; Spiering, M.J. Symbioses of grass with seed borne fungal endophytes. Annu. Rev. Plant Biol. 2004, 55, 315–340. [Google Scholar] [CrossRef]
- Liang, Y.; Wang, H.; Li, C.; Nan, Z.; Li, F. Effects of feeding drunken horse grass infected with Epichloë gansuensis endophyte on animal performance, clinical symptoms and physiological parameters in sheep. Bmc Vet. Res. 2017, 13, 223. [Google Scholar] [CrossRef] [Green Version]
- Reddy, P.; Deseo, M.A.; Ezernieks, V.; Guthridge, K.; Spangenberg, G.; Rochfort, S. Toxic indole diterpenes from endophyte-infected perennial ryegrass Lolium perenne L.: Isolation and stability. Toxins 2019, 11, 16. [Google Scholar] [CrossRef] [Green Version]
- Young, C.A.; Hume, D.E.; McCulley, R.L. Forages and pastures symposium: Fungal endophytes of tall fescue and perennial ryegrass: Pasture friend or foe? J. Anim. Sci. 2013, 91, 2379–2394. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dapprich, P.; Paul, V.; Krohn, K. Incidence of Acremonium endophytes in selected German pastures and the contents of alkaloids in Lolium perenne. IOBC WPRS Bull. 1996, 19, 103. [Google Scholar]
- Lewis, G.C.; Ravel, C.; Naffaa, W.; Astier, C.; Charmet, G. 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. 1997, 130, 227–238. [Google Scholar] [CrossRef]
- Zabalgogeazcoa, I.; Bony, S. Neotyphodium research and application in Europe. In Neotyphodium in Cool-Season Grasses; John Wiley & Sons Ltd; Blackwell Publishing: Oxford, UK, 2008; pp. 23–33. ISBN 978-0-470-38491-6. [Google Scholar]
- Fletcher, L.R.; Harvey, I.C. An Association of a Lolium Endophyte with Ryegrass Staggers. N. Z. Vet. J. 1981, 29, 185–186. [Google Scholar] [CrossRef] [PubMed]
- Reed, K.F.M.; Nie, Z.N.; Walker, L.V.; Mace, W.J.; Clark, S.G. Weather and pasture characteristics associated with outbreaks of perennial ryegrass toxicosis in southern Australia. Anim. Prod. Sci. 2011, 51, 738. [Google Scholar] [CrossRef]
- Odriozola, E.; Lopez, T.; Campero, C.; Gimenez, C.P. Ryegrass staggers in heifers: A new mycotoxicosis in Argentina. Vet. Hum. Toxicol. 1993, 35, 144–146. [Google Scholar]
- Butendieck, B.; Romero, Y.; Hazard, T.; Mardones, M.; Galdames, G. Caida del consumo y produccion de leche en vacas alimentadas con Lolium perenne infectada con Acremonium lolii [Drop in intake and milk production of cows fed with Lolium perenne infected with Acremonium lolii]. Agric. Técnica (Santiago) 1994, 54, 1–6. [Google Scholar]
- Benkhelil, A.; Grancher, D.; Giraud, N.; Et, P.B.; Bony, S. Intoxication par des toxines de champignons endophytes chez des taureaux reproducteurs. Rev. Méd. Vét. 2004, 156, 243–247. [Google Scholar]
- Christensen, M.J.; Leuchtmann, A.; Rowan, D.D.; Tapper, B.A. Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (Festuca pratensis) and perennial ryegrass (Lolium perenne). Mycol. Res. 1993, 97, 1083–1092. [Google Scholar] [CrossRef]
- Takach, J.E.; Mittal, S.; Swoboda, G.A.; Bright, S.K.; Trammell, M.A.; Hopkins, A.A.; Young, C.A. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl. Environ. Microbiol. 2012, 78, 5501–5510. [Google Scholar] [CrossRef] [Green Version]
- Finch, S.C.; Fletcher, L.R.; Babu, J.V. The evaluation of endophyte toxin residues in sheep fat. N. Z. Vet. J. 2012, 60, 56–60. [Google Scholar] [CrossRef] [PubMed]
- Finch, S.C.; Thom, E.R.; Babu, J.V.; Hawkes, A.D.; Waugh, C.D. The evaluation of fungal endophyte toxin residues in milk. N. Z. Vet. J. 2013, 61, 11–17. [Google Scholar] [CrossRef] [PubMed]
- Campbell, M.A.; Tapper, B.A.; Simpson, W.R.; Johnson, R.D.; Mace, W.; Ram, A.; Lukito, Y.; Dupont, P.-Y.; Johnson, L.J.; Scott, D.B.; et al. Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy. Mycologia 2017, 109, 715–729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ludlow, E.J.; Vassiliadis, S.; Ekanayake, P.N.; Hettiarachchige, I.K.; Reddy, P.; Sawbridge, T.I.; Rochfort, S.J.; Spangenberg, G.C.; Guthridge, K.M. Analysis of the indole diterpene gene cluster for biosynthesis of the epoxy-janthitrems in Epichloë endophytes. Microorganisms 2019, 7, 560. [Google Scholar] [CrossRef] [Green Version]
- Reddy, P.; Elkins, A.; Hemsworth, J.; Guthridge, K.; Vassiliadis, S.; Read, E.; Spangenberg, G.; Rochfort, S. Identification and distribution of novel metabolites of lolitrem B in mice by high-resolution mass spectrometry. Molecules 2020, 25, 372. [Google Scholar] [CrossRef] [Green Version]
- Hennessy, L.M.; Popay, A.J.; Finch, S.C.; Clearwater, M.J.; Cave, V.M. Temperature and plant genotype alter alkaloid concentrations in ryegrass infected with an Epichloë endophyte and this affects an insect herbivore. Front. Plant Sci. 2016, 7, 1097. [Google Scholar] [CrossRef]
- Babu, J.V.; Popay, A.J.; Miles, C.O.; Wilkins, A.L.; di Menna, M.E.; Finch, S.C. Identification and structure elucidation of janthitrems A and D from Penicillium janthinellum and determination of the tremorgenic and anti-insect activity of janthitrems A and B. J. Agric. Food Chem. 2018, 66, 13116–13125. [Google Scholar] [CrossRef]
- Aiken, G.E.; Strickland, J.R. Forages and pastures symposium: Managing the tall fescue–fungal endophyte symbiosis for optimum forage-animal production. J. Anim. Sci. 2013, 91, 2369–2378. [Google Scholar] [CrossRef]
- Repussard, C.; Zbib, N.; Tardieu, D.; Guerre, P. Endophyte infection of tall fescue and the impact of climatic factors on ergovaline concentrations in field crops cultivated in southern France. J. Agric. Food Chem. 2014, 62, 9609–9614. [Google Scholar] [CrossRef]
- Easton, S.; Tapper, B. Neotyphodium research and application in New Zealand. In Neotyphodium in Cool-Season Grasses; Wiley-Blackwell: Oxford, UK, 2008; pp. 35–42. ISBN 978-0-470-38491-6. [Google Scholar]
- Vikuk, V.; Young, C.A.; Lee, S.T.; Nagabhyru, P.; Krischke, M.; Mueller, M.J.; Krauss, J. Infection rates and alkaloid patterns of different grass species with systemic Epichloë endophytes. Appl. Environ. Microbiol. 2019, 85, e00465-19. [Google Scholar] [CrossRef] [Green Version]
- Johnson, L.J.; de Bonth, A.C.M.; Briggs, L.R.; Caradus, J.R.; Finch, S.C.; Fleetwood, D.J.; Fletcher, L.R.; Hume, D.E.; Johnson, R.D.; Popay, A.J.; et al. The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers. 2013, 60, 171–188. [Google Scholar] [CrossRef]
- Karpyn Esqueda, M.; Yen, A.L.; Rochfort, S.; Guthridge, K.M.; Powell, K.S.; Edwards, J.; Spangenberg, G.C. A review of perennial ryegrass endophytes and their potential use in the management of African Black Beetle in perennial grazing systems in Australia. Front. Plant Sci. 2017, 8, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stewart, A.V. Genetic origins perennial ryegrass. In Proceedings of the 13th Australasian Plant Breeding Conference, Christchurch, New Zealand, 18–21 April 2006; pp. 11–20. [Google Scholar]
- Hume, D.E.; Stewart, A.V.; Simpson, W.R.; Johnson, R.D. Epichloë fungal endophytes play a fundamental role in New Zealand grasslands. J. R. Soc. N. Z. 2020, 1–20. [Google Scholar] [CrossRef]
- Bundessortenamt. Beschreibende Sortenliste Futtergräser, Esparsette, Klee, Luzerne 2016; Bundessortenamt: Hannover, Germany, 2016; ISSN 16 12–89 4X. [Google Scholar]
- Bundessortenamt. Beschreibende Sortenliste Rasengräser 2017—Describing Variety List of Lawn Grasses 2017; Bundessortenamt: Hannover, Germany, 2017; ISSN 14 30–97 85. [Google Scholar]
- Leyronas, C.; Raynal, G. Presence of Neotyphodium-like endophytes in European grasses. Ann. Appl. Biol. 2001, 139, 119–127. [Google Scholar] [CrossRef]
- Saikkonen, K.; Ahlholm, J.; Helander, M.; Lehtimaki, S.; Niemelainen, O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography 2000, 23, 360–366. [Google Scholar] [CrossRef]
- Jensen, A.M.D. Endophyte persistence and toxin (lolitrem b) production in a Danish seed crop of perennial ryegrass. Eur. J. Agron. 2005, 23, 68–78. [Google Scholar] [CrossRef]
- Fuchs, B.; Krischke, M.; Mueller, M.J.; Krauss, J. Peramine and lolitrem B from endophyte-grass associations cascade up the food chain. J. Chem. Ecol. 2013, 39, 1385–1389. [Google Scholar] [CrossRef]
- König, J.; Fuchs, B.; Krischke, M.; Mueller, M.J.; Krauss, J. Hide and seek—Infection rates and alkaloid concentrations of Epichloё festucae var. lolii in Lolium perenne along a land-use gradient in Germany. Grass Forage Sci. 2018, 73, 510–516. [Google Scholar]
- Rudolph, W.; Remane, D.; Wissenbach, D.K.; Peters, F.T. Development and validation of an ultrahigh performance liquid chromatography-high resolution tandem mass spectrometry assay for nine toxic alkaloids from endophyte-infected pasture grasses in horse serum. J. Chromatogr. A 2018, 1560, 35–44. [Google Scholar] [CrossRef]
- Craig, A.M.; Blythe, L.L.; Duringer, J.M. The role of the Oregon State University Endophyte Service Laboratory in diagnosing clinical cases of endophyte toxicoses. J. Agric. Food Chem. 2014, 62, 7376–7381. [Google Scholar] [CrossRef]
- Ju, H.-J.; Hill, N.S.; Abbott, T.; Ingram, K.T. Temperature influences on endophyte growth in tall fescue. Crop Sci. 2006, 46, 404–412. [Google Scholar] [CrossRef]
- Rudgers, J.A.; Swafford, A.L. Benefits of a fungal endophyte in Elymus virginicus decline under drought stress. Basic Appl. Ecol. 2009, 10, 43–51. [Google Scholar] [CrossRef]
- Bourguignon, M.; Nelson, J.A.; Carlisle, E.; Ji, H.; Dinkins, R.D.; Phillips, T.D.; McCulley, R.L. Ecophysiological responses of tall fescue genotypes to fungal endophyte infection, elevated temperature, and precipitation. Crop Sci. 2015, 55, 2895–2909. [Google Scholar] [CrossRef] [Green Version]
- Bastias, D.A.; Martinez-Ghersa, M.A.; Ballare, C.L.; Gundel, P.E. Epichloë fungal endophytes and plant defenses: Not just alkaloids. Trends Plant Sci. 2017, 22, 939–948. [Google Scholar] [CrossRef] [PubMed]
- Dupont, P.-Y.; Eaton, C.J.; Wargent, J.J.; Fechtner, S.; Solomon, P.; Schmid, J.; Day, R.C.; Scott, B.; Cox, M.P. Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. N. Phytol. 2015, 208, 1227–1240. [Google Scholar] [CrossRef] [PubMed]
- Schardl, C.L. Epichloë species: Fungal symbionts of grasses. Annu. Rev. Phytopathol. 1996, 34, 109–130. [Google Scholar] [CrossRef]
- Soto-Barajas, M.C.; Vázquez-de-Aldana, B.R.; Álvarez, A.; Zabalgogeazcoa, I. Sympatric Epichloë species and chemotypic profiles in natural populations of Lolium perenne. Fungal Ecol. 2019, 39, 231–241. [Google Scholar] [CrossRef]
- Zabalgogeazcoa, I.; De Aldana, B.R.V.; Criado, B.G.; Ciudad, A.G. The infection of Festuca rubra by the fungal endophyte Epichloë festucae in Mediterranean permanent grasslands. Grass Forage Sci. 1999, 54, 91–95. [Google Scholar] [CrossRef]
- Bauer, J.I.; Gross, M.; Cramer, B.; Humpf, H.-U.; Hamscher, G.; Usleber, E. Immunochemical analysis of paxilline and ergot alkaloid mycotoxins in grass seeds and plants. J. Agric. Food Chem. 2018, 66, 315–322. [Google Scholar] [CrossRef]
- Pirelli, G.J.; Anderson, N.P.; Craig, A.M.; Young, C.A. Endophyte toxins in grass and other feed sources—Risks to livestock. Or. State Univ. Ext. Serv. 2016, EM9156, 1–10. [Google Scholar]
ID | Perennial Ryegrass Varieties | Tall Fescue Varieties | Other Grass Species | Product |
---|---|---|---|---|
S_10 | 50% BARCLAY II, 25% BAREURO, 25% BARMINTON | - | - | Regenerations-Mischung RPR, Eurogreen (T) |
S_11 | Unknown variety in unknown percentage | - | Poa pratensis, Festuca pratensis, Dactylis glomerata, Phleum pratense, Festuca rubra, Agrostis | Gräsermischung Weidesaat, Kräuterwiese (F) |
S_12 | 25% lawn type, unknown variety 25% pasture type, unknown variety | - | 20% Poa pratensis, 20% Phleum pratense, 10% Festuca rubra | Country Horse 2117, DSV (F) |
S_13 | 10% CARNAC, 18% CLEOPATRA, 10% DICKENS, 1% EURODIAMOND, 7% DOUBLE 4n, 8% FABIAN 4n, 5% CORSICA, 7% SIRTAKY/SHORTY, 10% ZÜRICH | - | 25% Poa pratensis | Regeneration Highspeed, UFA (T) |
S_14 | - | 100% LIPALMA | - | Camena Samen (F) |
S_15 | 33% MATHILDE, 34% WADI, 33% BELIDA | - | - | Elite Gvo, Rudloff (F) |
S_16 | 20% EURODIAMOND, 15% SIRTAKY | 15% BARCESAR, 35% MEANDRE | 15% Poa pratensis | Reitbahn, UFA (T) |
S_17 | 25% DISCUS | 20% LIPALMA | 25% Festuca pratensis, 20% Phleum pratense, 10% Poa pratensis | Country Öko 2117, DSV (F) |
S_18 | 15% BOYNE, 20% TODDINGTON, 20% INDICUS 1, 15% POLIM, 15% ARUSI, 15% GARBOR | - | - | Profi Nachsaat Gvo, HaGe Kiel (F) |
S_19 | 100% KARATOS | - | - | Camena Samen (F) |
S_20 | - | - | 7% Agrostis capillaris, 3% Alopecurus pratensis, 12% Arrhenatherum elatius, 10% Cynosurus cristatus, 10% Dactylis glomerata, 15% Festuca rubra, 1% Holcus lanatus, 13% Phleum pratense, 18% Poa pratensis, 1% Trisetum flavescens | Heuwiese für Pferde, Appels Wilde Samen (F) |
S_21 | 10% KARATOS, 20% KUBUS, 15% TWYMAX | - | 25% Phleum pratense, 12% Poa pratensis, 15% Festuca rubra | Pferdeweide 1, Camena Samen (F) |
S_22 | 8% PREMIUM | - | 18% Festulolium, 18% Phleum pratense, 15% Festuca pratensis | Rotkleegras 91, Camena Samen (F) |
S_23 | 100% POLIM | - | - | Camena Samen (F) |
S_24 | 12% BELLEVUE, 20% BOYNE, 40% STEFANI | - | 18% Phleum pratense, 10% Poa pratensis | Pferdeweide Nachsaat, Raiffeisen (F) |
S_25 | 20% IVANA, 10% TIVOLI, 20% SW BIRGER | 20% SWAJ | 10% Poa pratensis, 20% Phleum pratense | Pferdegreen Öko PR940, BSV Saaten (F) |
S_26 | 100% TWYMAX | - | - | Camena Samen (F) |
S_27 | 28% MATHILDE, 23% ALFAN, 13% BELIDA | - | 10% Festuca pratensis, 5% Poa pratensis, 21% Phleum pratense | Elite 20, Rudloff (F) |
S_28 | 25% MARAVA, 30% BOKSER, 30% WADI | - | 15% Phleum pratense | Equitana Nachsaat Gvo, Rudloff (F) |
S_29 | 10% DOUBLE | 45% BARCESAR, 25% DEBUSSY 1 | 20% Poa pratensis | Monaco-Mischung RSM, Eurogreen (T) |
S_30 | 11% TREND, 10% TWYMAX, 5% KARATOS | - | 10% Festuca pratensis, 11% Festulolium fedoro, 7% Dactylis glomerata, 5% Poa pratensis, 5% Festuca rubra, 14% Phleum pratense | Kräuterweide, Camena Samen (F) |
S_31 | Unknown variety in unknown percentage | - | Festuca pratensis, Poa pratensis, Poa trivialis, Festuca rubra, Phleum pratense, Alopecurus pratensis, Cynosurus cristatus, Elymus repens | Pferdeweide-Reparatursaat, Kräuterwiese (F) |
S_32 | 15% MARAVA, 15% BOKSER, 15% WADI | - | 25% Phleum pratense, 20% Poa pratensis, 10% Festuca rubra | Equitana Universal, Rudloff (F) |
S_33 | 5% COLUMBINE, 6% DOUBLE 4 n, 6% FABIAN 4n, 12% MERCITWO, 5% NEW ORLEANS, 11% SIRTAKY | - | 40% Poa pratensis, 15% Festuca rubra | Primera Highspeed, UFA (T) |
Endophyte Detection Noble Research Institute | Alkaloid Detection [ppb] | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
University of Würzburg | Oregon State University | ||||||||||
First Screen | Second Screen | Total [%] | Ergovaline | Lolitrem B | Paxilline | Peramine | Ergovaline | Lolitrem B | |||
ID | #Seeds | E+ | #Seeds | E+ | |||||||
S_10 | 24 | 3 | 24 | 0 | 6.3 | 435 | 851 | 1540 | 1899 | 844 | 1688 |
S_11 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 # | |
S_12 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | - | |
S_13 | 22 | 1 | 24 | 0 | 2.2 | nd | nd | nd | 10 | <100 | <100 |
S_14 | 24 | 0 | 24 | 0 | nd | nd | nd | <10 | <100 | <100 | |
S_15 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_16 | 24 | 2 | 24 | 1 | 6.3 | nd | nd | nd | 65 | <100 | 104 |
S_17 | 22 | 0 | 22 | 0 | nd | nd | nd | <10 | <100 | <100 | |
S_18 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_19 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_20 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_21 | 22 | 0 | 22 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_22 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_23 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | - | |
S_24 | 24 | 3 | 24 | 0 | 6.3 | 709 | 240 | nd | 2286 | 425 | 991 |
S_25 | 22 | 0 | 22 | 0 | nd | nd | nd | nd | <100 | <100 # | |
S_26 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_27 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_28 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | - | |
S_29 | 22 | 0 | 22 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_30 | 24 | 0 | 24 | 1 | 2.1 | nd | nd | nd | nd | <100 | <100 # |
S_31 | 24 | 0 | 24 | 0 | nd | nd | nd | nd | <100 | <100 | |
S_32 | 24 | 0 | 24 | 0 | 335 | 494 | nd | 1507 | 287 | 725 | |
S_33 | 22 | 2 | 22 | 2 | 8.7 | 7 | nd | nd | 40 | 166 | 372 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Krauss, J.; Vikuk, V.; Young, C.A.; Krischke, M.; Mueller, M.J.; Baerenfaller, K. Epichloë Endophyte Infection Rates and Alkaloid Content in Commercially Available Grass Seed Mixtures in Europe. Microorganisms 2020, 8, 498. https://doi.org/10.3390/microorganisms8040498
Krauss J, Vikuk V, Young CA, Krischke M, Mueller MJ, Baerenfaller K. Epichloë Endophyte Infection Rates and Alkaloid Content in Commercially Available Grass Seed Mixtures in Europe. Microorganisms. 2020; 8(4):498. https://doi.org/10.3390/microorganisms8040498
Chicago/Turabian StyleKrauss, Jochen, Veronika Vikuk, Carolyn A. Young, Markus Krischke, Martin J. Mueller, and Katja Baerenfaller. 2020. "Epichloë Endophyte Infection Rates and Alkaloid Content in Commercially Available Grass Seed Mixtures in Europe" Microorganisms 8, no. 4: 498. https://doi.org/10.3390/microorganisms8040498