Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra)
P. E. Gundel A B D , I. Zabalgogeazcoa C and B. R. Vázquez de Aldana CA IFEVA-Facultad de Agronomía (UBA)/CONICET, Cátedra de Ecología, Av. San Martín 4453 (C1417DSE), Buenos Aires, Argentina.
B MTT Agrifood Research Finland, Plant Protection, 31600 Jokioinen, Finland.
C Instituto de Recursos Naturales y Agrobiología de Salamanca, IRNASA-CSIC, Apartado 257, 37071 Salamanca, Spain.
D Corresponding author. Email: gundel@agro.uba.ar
Crop and Pasture Science 62(11) 1010-1016 https://doi.org/10.1071/CP11300
Submitted: 4 May 2011 Accepted: 11 November 2011 Published: 13 December 2011
Abstract
In diverse natural habitats of Europe, plants of Festuca rubra are commonly infected by the fungal endophyte Epichloë festucae. Under several circumstances, the association between the grass and the fungus has been shown to be mutualistic. Here, we conducted an experiment to study the differences in seed germination and mortality between infected (E+) and endophyte-free plants (E–) at different temperatures (12 and 25°C) and water potentials (0 and –0.5 MPa). Three half-sib lines of F. rubra, each composed of E+ and E– seeds, and derived from infected plants from semiarid grasslands were used. Although the endophyte effect depended on the incubation condition, germination percentage was significantly greater for E– (52%) than for E+ seeds (41%). Seed germination was more inhibited by the low water potential (75 v. 24% for –0.5 and 0.0 MPa, respectively), than by the high temperature (64 v. 35% for 25 and 12°C, respectively). However, mortality was highly dependent on the interaction between plant genotype and endophyte, and between temperature and water condition. It is remarkable that while highly dependent on the host genotype, there was a clear effect of endophyte increasing seed survival, especially in those treatments that were unfavourable for germination. For example, in the more restrictive treatment (25°C and –0.5 MPa), seed survival was on average, 44 and 39% for E+ and E–, respectively. In general, the endophyte affected seed characteristics of F. rubra by reducing the percentage of germination, but simultaneously increasing seed survival.
Additional keywords: dehesas, grasslands, plant–endophyte symbiosis, seed germination, seed survival, symbiotic interaction.
References
Ahlholm JU, Helander M, Lehtimäki S, Wäli P, Saikkonen K (2002) Vertically transmitted fungal endophytes: different responses of host–parasite systems to environmental conditions. Oikos 99, 173–183.| Vertically transmitted fungal endophytes: different responses of host–parasite systems to environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Allen PS, Meyer SE, Khan MA (2000) Hydrothermal time as a tool in comparative germination studies. In ‘Seed biology: advances and applications’. (Eds M Black, KJ Bradford, J Vázquez-Ramos) pp. 401–410. (CABI Publishing: Wallingford, UK)
Arroyo García R, Martínez Zapater JM, García Criado B, Zabalgogeazcoa I (2002) The genetic structure of natural populations of the fungal endophyte Epichloë festucae. Molecular Ecology 11, 355–364.
| The genetic structure of natural populations of the fungal endophyte Epichloë festucae.Crossref | GoogleScholarGoogle Scholar |
Bacon CW, White JF, Jr (1994) Stains, media, and procedures for analyzing endophytes. In ‘Biotechnology of endophytic fungi of grasses’. (Eds CW Bacon, JF White Jr) pp. 47–56. (CRC: Boca Raton, FL)
Bazely DR, Ball JP, Vicari M, Tanentzap AJ, Bérenger M, Rakocevic T, Koh S (2007) Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses. Ecography 30, 367–374.
| Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses.Crossref | GoogleScholarGoogle Scholar |
Benech-Arnold RL, Sánchez RA, Forcella F, Kruk BC, Ghersa CM (2000) Environmental control of dormancy in weed seed soil banks. Field Crops Research 67, 105–122.
| Environmental control of dormancy in weed seed soil banks.Crossref | GoogleScholarGoogle Scholar |
Bradford KJ (2002) Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Research 50, 248–260.
Brar GS, Palazzo AJ (1997) Temperature and germination relationships of Festuca varieties. Plant Varieties and Seeds 10, 103–111.
Brilman LA (2005) Endophytes in turfgrass cultivars. In ‘Neotyphodium in cool season grasses’. (Eds CA Roberts, CP West, DE Spiers) pp. 341–349. (Blackwell Publishing: Ames, IA)
Cheplick GP (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environmental and Experimental Botany 60, 202–210.
| Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation.Crossref | GoogleScholarGoogle Scholar |
Clarke BB, White JF, Hurley H, Torres MS, Sun S, Huff DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Disease 90, 994–998.
| Endophyte-mediated suppression of dollar spot disease in fine fescues.Crossref | GoogleScholarGoogle Scholar |
Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160, S99–S127.
| Evolutionary origins and ecological consequences of endophyte symbiosis with grasses.Crossref | GoogleScholarGoogle Scholar |
Easton HS (2007) Grasses and Neotyphodium endophytes: co-adaptation and adaptive breeding. Euphytica 154, 295–306.
| Grasses and Neotyphodium endophytes: co-adaptation and adaptive breeding.Crossref | GoogleScholarGoogle Scholar |
Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecology Letters 7, 304–313.
| Asexual Neotyphodium endophytes in a native grass reduce competitive abilities.Crossref | GoogleScholarGoogle Scholar |
Gundel PG, Maseda PH, Vila-Aiub MM, Ghersa CM, Benech-Arnold RL (2006) Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability. Annals of Botany 97, 571–577.
| Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287ltVOntw%3D%3D&md5=1eaaccbabb5171aa9468a1d8a4932821CAS |
Gundel PE, Martínez-Ghersa MA, Garibaldi LA, Ghersa CM (2009) Viability of Neotyphodium endophytic fungus and endophyte-infected and noninfected Lolium multiflorum seeds. Botany 87, 88–96.
| Viability of Neotyphodium endophytic fungus and endophyte-infected and noninfected Lolium multiflorum seeds.Crossref | GoogleScholarGoogle Scholar |
Gundel PE, Martínez-Ghersa MA, Batista WB, Ghersa CM (2010) Dynamics of Neotyphodium endophyte infection in ageing seed pools: incidence of differential viability loss of endophyte, infected seed, and non-infected seed. Annals of Applied Biology 156, 199–209.
| Dynamics of Neotyphodium endophyte infection in ageing seed pools: incidence of differential viability loss of endophyte, infected seed, and non-infected seed.Crossref | GoogleScholarGoogle Scholar |
Harper JL (1977) ‘Population biology of plants.’ (Academic Press: London)
Larsen SU, Bibby BM (2005) Differences in thermal time requirement for germination of three turfgrass species. Crop Science 45, 2030–2037.
| Differences in thermal time requirement for germination of three turfgrass species.Crossref | GoogleScholarGoogle Scholar |
Leuchtmann A, Schardl CL, Siegel MR (1994) Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses. Mycologia 86, 802–812.
| Sexual compatibility and taxonomy of a new species of Epichloë symbiotic with fine fescue grasses.Crossref | GoogleScholarGoogle Scholar |
Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Science 40, 923–940.
| Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXns1Gqsb8%3D&md5=d76f3bcb906e0be892c5be18eddd598cCAS |
Marks S, Clay K (2007) Low resource availability differentially affects the growth of host grasses infected by fungal endophytes. International Journal of Plant Sciences 168, 1269–1277.
| Low resource availability differentially affects the growth of host grasses infected by fungal endophytes.Crossref | GoogleScholarGoogle Scholar |
Martínez-Ghersa MA, Ghersa CM, Benech-Arnold RL, MacDonough R, Sánchez RA (2000) Adaptive traits regulating dormancy and germination of invasive species. Plant Species Biology 15, 127–137.
| Adaptive traits regulating dormancy and germination of invasive species.Crossref | GoogleScholarGoogle Scholar |
Michel BE (1983) Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiology 72, 66–70.
| Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktFyqtbw%3D&md5=610dda91b5f32c419904c5392713a52eCAS |
Morrison DA, Morris EC (2000) Pseudoreplication in experimental designs for the manipulation of seed germination treatments. Austral Ecology 25, 292–296.
| Pseudoreplication in experimental designs for the manipulation of seed germination treatments.Crossref | GoogleScholarGoogle Scholar |
Neil KL, Tiller RL, Faeth SH (2003) Big sacaton and endophyte-infected Arizona fescue germination under water stress. Journal of Range Management 56, 616–622.
| Big sacaton and endophyte-infected Arizona fescue germination under water stress.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2010) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at: www.R-project.org
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=f5caf17794b855cee54b142dbddb0883CAS |
Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Annals of Botany 98, 379–387.
| Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration.Crossref | GoogleScholarGoogle Scholar |
Vázquez de Aldana BR, García-Ciudad A, García-Criado B (2008) Interannual variations of above-ground biomass and nutritional quality of Mediterranean grasslands in Western Spain over a 20-year period. Australian Journal of Agricultural Research 59, 769–779.
| Interannual variations of above-ground biomass and nutritional quality of Mediterranean grasslands in Western Spain over a 20-year period.Crossref | GoogleScholarGoogle Scholar |
Vázquez de Aldana BR, Zabalgogeazcoa I, Rubio de Casas R, García Ciudad A, García Criado B (2010) Relationships between the genetic distance of Epichloë festucae isolates and the ergovaline and peramine content of their Festuca rubra hosts. Annals of Applied Biology 156, 51–61.
| Relationships between the genetic distance of Epichloë festucae isolates and the ergovaline and peramine content of their Festuca rubra hosts.Crossref | GoogleScholarGoogle Scholar |
Wäli PR, Helander M, Saloniemi I, Ahlholm J, Saikkonen K (2009) Variable effects of endophytic fungus on seedling establishment of fine fescues. Oecologia 159, 49–57.
| Variable effects of endophytic fungus on seedling establishment of fine fescues.Crossref | GoogleScholarGoogle Scholar |
White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiologia Plantarum 138, 440–446.
| Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOkt7Y%3D&md5=3fbe9e8718cd6fa028b02e87e6a42d0eCAS |
Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions 13, 1027–1033.
| Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntVaku7c%3D&md5=5ac1ab28aa0256174f59f46236b32e6fCAS |
Zabalgogeazcoa I, Vázquez de Aldana BR, García Criado B, García Ciudad A (1999) The infection of Festuca rubra by the endophyte Epichloë festucae in Mediterranean permanent grasslands. Grass and Forage Science 54, 91–95.
| The infection of Festuca rubra by the endophyte Epichloë festucae in Mediterranean permanent grasslands.Crossref | GoogleScholarGoogle Scholar |
Zabalgogeazcoa I, García Ciudad A, Vázquez de Aldana BR, García Criado B (2006a) Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra. European Journal of Agronomy 24, 374–384.
| Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Kitbg%3D&md5=8095aaafab8b2c2694ceaa70ef6de237CAS |
Zabalgogeazcoa I, Romo M, Keck E, Vázquez de Aldana BR, García Ciudad A, García Criado B (2006b) The infection of Festuca rubra subsp. pruinosa by Epichloë festucae. Grass and Forage Science 61, 71–76.
| The infection of Festuca rubra subsp. pruinosa by Epichloë festucae.Crossref | GoogleScholarGoogle Scholar |
Zabalgogeazcoa I, García Ciudad A, Leuchtmann A, Vázquez de Aldana BR, García Criado B (2008) Effects of choke disease in the grass Brachypodium phoenicoides. Plant Pathology 57, 467–472.
| Effects of choke disease in the grass Brachypodium phoenicoides.Crossref | GoogleScholarGoogle Scholar |