Abstract
Aims
Novel fungal endophyte (Neotyphodium coenophialum; Latch, Christensen and Samuels; Glenn, Bacon, and Hanlin) genotypes in symbiosis with tall fescue (Lolium arundinaceum; Schreb. Darbysh.) have been recently introduced to agricultural seed markets. These novel endophytes do not produce the full suite of toxins that the ‘common toxic’ form does, and therefore, may not have the same consequences on plant and soil processes. Here, we evaluated the effects of endophyte presence and genotype on ecosystem processes of tall fescue stands.
Methods
We quantified the effects of the presence of the common toxic endophyte (CT), two novel endophyte genotypes (AR-542, AR-584), no endophyte (endophyte free, E-), and a mixture of all endophyte statuses (mix) within a single genotype of tall fescue (PDF) on various soil and plant parameters.
Results
Endophyte presence and genotype affected tall fescue cover and plant species diversity: cover—CT, AR-542, AR -584, mix > E- and species diversity—E- > AR-542, AR -584 > CT, mix. Most measured soil parameters had significant endophyte effects. For example, higher fluxes of soil CO2 and N2O were measured from stands of AR-542 than from the other endophyte treatments.
Conclusions
These results indicate that endophyte presence and genetic identity are important in understanding the ecosystem-scale effects of this agronomically important grass-fungal symbiosis.
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References
Antonovics J (1992) Towards community genetics. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. Chicago Univ. Press, pp 426–449
Ball DM, Pedersen JF, Lacefield GD (1993) The tall-fescue endophyte. Am Sci 81:370–379
Belesky DP, Bacon CW (2009) Tall fescue and associated mutualistic toxic fungal endophytes in agroecosystems. Toxin Rev 28:102–117
Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, Watson RH, Parish JA, Hawkins LL, Thompson FN (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J 94:567–574
Bukovinszky T, Frank van Veen FJ, Jongema Y, Dickel M (2008) Direct and indirect effects of resource quality on food web structure. Science 319:804–807
Bultman TL, Bell GD (2003) Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos 103:182–190
Bultman TJ, Bell G, Martin WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685
Burns JC, Fisher DS (2010) Intake and digestibility of improved selections of tall fescue and orchardgrass hays. Crop Sci 50:419–426
Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7
Buyer JS, Zuberer DA, Nichols KA, Franzluebbers AJ (2011) Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil 339:401–412
Castellano MJ, Schmidt JP, Kaye JP, Walker C, Graham CB, Lin H, Dell C (2010) Hydrological and biogeochemical controls on the timing and magnitude of nitrous oxide flux across an agricultural landscape. Glob Change Biol 16:2711–2720
Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127
Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744
Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Nat Acad Sci 102:12465–12470
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968
Daubenmire RF (1959) A canopy coverage method. Northwest Science 33:43–64
Flynn ES, Dougherty CT, Wendroth O (2008) Assessment of pasture biomass with the Normalized Difference Vegetation Index from active ground-based sensors. Agron J 100:114–121
Franzluebbers AJ, Nazih N, Stuedemann JA, Fuhrmann JJ, Schomberg HH, Hartel PG (1999) Soil carbon and nitrogen pools under low- and high-endophyte infected tall fescue. Soil Sci Soc Am J 63:1687–1694
Gibson DJ, Colquhoun IA, Greig-Smith P (1985) A new method for measuring nutrient supply rates in soils using ion-exchange resins. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil: plants, microbes, and animals. Blackwell Scientific, Oxford, pp 73–79
Handayani IP, Coyne MS, Phillips TD (2011) Soil organic carbon fractions differ in two contrasting tall fescue systems. Plant Soil 338:43–50
Hiatt EE, Hill NS, Bouton JH, Stuedemann JA (1999) Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Sci 39:796–799
Hill NS, Belesky DP, Stringer WC (1998) Encroachment of endophyte infected on endophyte free tall fescue. Ann Bot 81:483–488
Hopkins AA, Young CA, Panaccione DG, Simpson WR, Mittal S, Bouton JH (2010) Agronomic performance and lamb health among several tall fescue novel endophyte combinations in the south-central USA. Crop Sci 50:1552–1561
Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623
Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. J Appl Ecol 42:762–769
Iqbal J, Siegrist JA, Nelson JA, McCulley RL (2012) Fungal endophyte infection increases carbon sequestration potential of Southeastern USA tall fescue stands. Soil Biol Biochem 44:81–92
Jenkins MB, Franzluebbers AJ, Humayoun SB (2006) Assessing short-term responses of prokaryotic communities in bulk and rhizosphere soils to tall fescue endophyte infection. Plant Soil 289:309–320
Kelrick MI, Kasper NA, Bultman TL, Taylor S (1990) Direct interactions between infected and uninfected individuals of Festuca arundinacea: differential allocation to shoot and root biomass. In: Quisenberry SS, Joost RE (eds) Proceedings of the International Symposium of Acremonium/grass interactions. Louisiana Agric Exp Station, New Orleans, pp 21–29
Latch GCM, Christensen MJ, Tapper BA, Easton HS, Hume DE, Fletcher LR (2000) Tall fescue endophytes. U.S. Patent 6 111 170. Date issued: 29 August
Lemons A, Clay K, Rudgers JA (2005) Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 145:595–604
Malinowski DP, Alloush GA, Belesky DP (1998) Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 205:1–12
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
Malinowski DP, Zuo H, Kramp BA, Muir JP, Pinchak WE (2005) Obligatory summer-dormant cool-season perennial grasses for semiarid environments of the Southern Great Plains. Agron J 97:147–154
McNear DH Jr, McCulley RL (2012) Influence of the Neotyphodium-tall fescue symbiosis on belowground processes. In: Young CA, Aiken GE, McCulley RL, Strickland JR, Schardl CL (eds) Epichloae, Endophytes of Cool Season Grasses: Implications, Utilization, and Biology. The Samuel Roberts Noble Foundation, Ardmore, pp 94–99
Orr SP, Rudgers JA, Clay K (2005) Invasive plants can inhibit native tree seedlings: testing potential allelopathic mechanisms. Plant Ecol 181:153–165
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 Nat Acad Sci 98:12820–12825
Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823
Rice CW, Smith MS, Crutchfield JM (1984) Inorganic N analysis of soil extracts by automated and distillation procedures. Comm Soil Sci Plant Anal 15(6):663–672
Rudgers JA, Fischer S, Clay K (2010) Managing plant symbiosis: fungal endophyte genotype alters plant community composition. J Appl Ecol 47:468–477
Rudgers JA, Holah J, Orr SP, Clay K (2007) Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88:18–25
Rudgers JA, Orr SP (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97:247–255
Shannon CE (1948) A mathematical theory of communication. Bell System Tech J 27:379–423 and 623–656
Siegrist JA, McCulley LR, Bush LP, Phillips TD (2010) Alkaloids may not be responsible for endophyte-associated reductions in tall fescue decomposition rates. Funct Ecol 24:460–468
Snow AA, Andow DA, Gepts P, Hallerman EM, Power A, Tiedje JM, Wolfenbarger LL (2005) Genetically engineered organisms and the environment: current status and recommendations. Ecol Appl 15:377–404
Soil and Plant Analysis Council Inc (2000) Soil analysis handbook of reference methods. CRC Press, Boca Raton
Stuedemann JA, Hoveland CS (1988) Fescue endophyte: history and impact on animal agriculture. J Prod Agric 1:39–44
Van Hecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:101–109
Waller JC, Fribourg HA, Carlisle RJ, Latch GCM, Fletcher LR, Hay RJM, Easton HS, Tapper BA (2000) Tall fescue with novel endophytes in Tennessee. Proceedings of the Fourth International Neotyphodium/Grass Interactions Symposium, Soest, Germany, p 142
Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL, Woolbright S, Kuske CR (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573
World Humanity Action Trust (2000) Governance for a sustainable future. A report by the World Humanity Action Trust. WHAT, London, http://www.earthsummit2002.org/es/issues/Governance/whatgov3.pdf
Acknowledgments
We thank Andy Hopkins, Carolyn Young, and the Noble Foundation for providing the tall fescue-fungal genotype seed and in helping to confirm the endophyte status of our plots. Thanks to Elizabeth Carlisle for her assistance in the field sampling and laboratory analysis. We also appreciate the help of R. Smith, A. Cooke, and L. Box for identifying and sorting plant species in the field. Funding for this project was provided via a cooperative agreement between the College of Agriculture at the University of Kentucky and the USDA-ARS Forage Animal Production Research Unit (58-6440-7-135) and the Kentucky Agricultural Experiment Station (KY006045).
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Fig. 1S
Comparison of spring season non-destructive cover estimates for (A) tall fescue (%), (B) other graminoid (%), (C) forb (%), and (D) woody plants (%) among treatments. Endophyte treatment descriptions are given in Fig. 1. Error bars indicate standard deviation of the mean (n = 6). Different letters indicate significant differences among treatments (as determined by Tukey’s test), and the P value is from the corresponding ANOVA model, with bolding indicating significance. There were no woody plants observed in the AR-542 treatment at this time (DOCX 69 kb)
Fig. 2S
Comparison of summer harvest for (A) total above ground biomass (g m−2), (B) tall fescue biomass (g m−2), (C) other graminoid biomass (g m−2), and (D) forb biomass (g m−2) among treatments. Treatment descriptions are given in Fig. 1. Error bars indicate standard deviation of the mean (n = 6). Treatment P-values taken from ANOVA models are shown (DOCX 80.5 kb)
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Iqbal, J., Nelson, J.A. & McCulley, R.L. Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soil 364, 15–27 (2013). https://doi.org/10.1007/s11104-012-1326-0
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DOI: https://doi.org/10.1007/s11104-012-1326-0