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Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma

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Abstract

This study was conducted to explore fungal endophyte communities inhabiting native switchgrass plants from the tallgrass prairie of northern Oklahoma. The primary focus was to isolate these endophytes in pure culture from surface-sterilized plant tissues and provide taxonomic identifications based on comparative analysis of ITS rDNA gene sequences. From these data, we evaluated the biodiversity of these potentially beneficial endosymbionts from this rapidly disappearing habitat of the Great Plains. While important from a strictly conservationist standpoint, this survey further allowed us to identify candidate endophytes for introduction into commercial switchgrass cultivars for biomass enhancement. A total of 210 whole plant samples were collected at early vegetative, full reproductive and senescence stages. Fungal endophytes were isolated, identified to species level when possible, and grouped into communities based on plant part, collection month and part of the prairie from which the plants were collected. Species diversity for each community was estimated by Shannon diversity index, and differences in diversity indices were compared using a t-test. The presence of fungal species representing at least 18 taxonomic orders suggests a high level of diversity in switchgrass endophyte communities. The fungal communities from shoot tissue had significantly higher species diversity than communities from the root tissue. The abundance of taxa assigned to the order Hypocreales (to which mutualistic, clavicipitaceous endophytes of cool-season grasses belong) found in shoot (64%) and root tissues (39%) throughout the growing season suggests great potential for utilizing these endophytes for enhancing biomass production and stress resistance of this important bioenergy crop.

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References

  • Abbott LK, Robson AL (eds) (1984) The effect of VA mycorrhizae on plant growth. CRC, Boca Raton

    Google Scholar 

  • Ahmad A, Alam M, Janardhanan KK (2001) Fungal endophyte enhances biomass production and essential oil yield of east Indian lemongrass. Symbiosis 30:275–285

    Google Scholar 

  • Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654

    Article  PubMed  CAS  Google Scholar 

  • Bisby FA, Roskov YR, Orrell TM, Nicolson D, Paglinawan LE, Bailly N, Kirk P, Bourgoin T, Baillargeon G (2010) Species 2000 and ITIS catalogue of life: 2010 annual checklist. Species 2000 Reading, UK

  • Bischoff KM, Wicklow DT, Jordan DB, de Rezende ST, Liu SQ, Hughes SR, Rich JO (2009) Extracellular hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr Microbiol 58:499–503

    Article  PubMed  CAS  Google Scholar 

  • Bouton J (2007) The economic benefits of forage improvement in the United States. Euphytica 154:263–270

    Article  Google Scholar 

  • Bouton J (2008) Improvement of switchgrass as a bioenergy crop. In: Vermerris W (ed), Genetic improvement of bioenergy crops. Springer Science and Business Media, pp 295–308

  • Bowman KO, Hutcheson K, Odum EP, Shenton LR (eds) (1971) Comments on distribution of indices of diversity. The Pennsylvania State University Press, University Park

    Google Scholar 

  • Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7

    PubMed  CAS  Google Scholar 

  • Choi GJ, Kim JC, Jang KS, Nam MH, Lee SW, Kim HT (2009) Biocontrol activity of Acremonium strictum BCP against Botrytis diseases. Plant Pathol J 25:165–171

    Article  Google Scholar 

  • Christensen MJ, Simpson WR, Al Samarrai T (2000) Infection of tall fescue and perennial ryegrass plants by combinations of different Neotyphodium endophytes. Mycol Res 104:974–978

    Article  Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    Article  PubMed  Google Scholar 

  • Clay K, Cheplick GP, Marks S (1989) Impact of fungus Balansia henningsiana on Panicum agrostoides: frequency of infection, plant growth and reproduction, and resistance to pests. Oecologia 80:374–380

    Article  Google Scholar 

  • de Jong EV, Dobrowolski MP, Bannan NR, Stewart AV, Smith KF, Spangenberg GC, Forster JW (2008) Global genetic diversity of the perennial ryegrass fungal endophyte Neotyphodium lolii. Crop Sci 48:1487–1501

    Article  Google Scholar 

  • Diehl WW (1950) Balansia and Balansiae in America. Agriculture Monograph No. 4. United States Department of Agriculture, Washington, p 82

    Google Scholar 

  • Dongyi H, Kelemu S (2004) Acremonium implicatum, a seed-transmitted endophytic fungus in Brachiaria grasses. Plant Dis 88:1252–1254

    Article  CAS  Google Scholar 

  • Evans JW (2006) Commercialization of AR1 in Australia. In: Popay AJ, Thom ER (eds) International symposium on fungal endophytes of grasses. New Zealand Grassland Association, Christchurch, pp 241–242

    Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidimycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  • George E, Marschner H, Jakobsen I (1995) Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit Rev Biotechnol 15:257–270

    Article  Google Scholar 

  • Ghimire SR, Charlton ND, Craven KD (2009) The mycorrhizal fungus, Sebacina vermifera, enhances seed germination and biomass production in switchgrass (Panicum virgatum L). Bioenerg Res 2:51–58

    Article  Google Scholar 

  • Groth JV, Roelfs AP (1987) The concept of measurement of phenotypic diversity in Puccinia graminis on wheat. Phytopathology 77:1395–1399

    Article  Google Scholar 

  • Hamilton RG (1996) Using fire and bison to restore a functional tallgrass prairie landscape, Transactions of the 61st North American Wildlife and Natural Resource Conference. Wildlife Management Institute Tulsa, Oklahoma, pp 208–214

    Google Scholar 

  • Horinouchi H, Muslim A, Suzuki T, Hyakumachi M (2007) Fusarium equiseti GF191 as an effective biocontrol agent against Fusarium crown and root rot of tomato in rock wool systems. Crop Prot 26:1514–1523

    Article  Google Scholar 

  • Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  • Kaur R, Kaur J, Singh RS (2010) Nonpathogenic Fusarium as a biological control agent. Plant Pathol J 9:88–100

    Google Scholar 

  • Kelemu S, White JF, Munoz F, Takayama Y (2001) An endophyte of the tropical forage grass Brachiaria brizantha: Isolating, identifying, and characterizing the fungus, and determining its antimycotic properties. Can J Microbiol 47:55–62

    Article  PubMed  CAS  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CABI, Wallingford, p 332

    Google Scholar 

  • Linderman RG, Hendrix JW (eds) (1982) Evaluation of plant response to colonization by vascular-arbuscular mycorrhizal fungi: a host variables. American Phytopathological Society, St. Paul

    Google Scholar 

  • Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology 5:28

    Article  PubMed  Google Scholar 

  • Milne GD (2006) Technology transfer of novel ryegrass endophyte in New Zealand. In: Popay AJ, Thom ER (eds) Internation symposium on fungal endophytes of grasses. New Zealand Grassland Association, Christchurch, pp 237–239

    Google Scholar 

  • National Park Service (2010) Last stand of the tallgrass prairie. Tallgrass Prairie National Preserve Cottonwood Falls, KS

    Google Scholar 

  • Neubert K, Mendgen K, Brinkmann H, Wirsel SGR (2006) Only a few fungal species dominate highly diverse mycofloras associated with the common reed. Appl Environ Microbiol 72:1118–1128

    Article  PubMed  CAS  Google Scholar 

  • Pedersen JF, Lacefield GD, Ball DM (1990) A review of the agronomic characteristics of endophyte free and endophyte infected tall fescue. Appl Agric Res 5:188–194

    Google Scholar 

  • Petrini O (1986) Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, Van Den Heuvel J (eds) Microbiology of the phyllosphere. Cambridge University Press, New York, pp 175–187

    Google Scholar 

  • Puckette M, Peal L, Steele J, Tang YH, Mahalingam R (2009) Ozone responsive genes in Medicago truncatula: analysis by suppression subtraction hybridization. J Plant Physiol 166:1284–1295

    Article  PubMed  CAS  Google Scholar 

  • Safir GR, Boyer JS (1971) Mycorrhizal enhancement of water transport in soybean. Science 172:581–583

    Article  PubMed  CAS  Google Scholar 

  • Sanchez Marquez S, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195

    Google Scholar 

  • Sanchez Marquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100

    Google Scholar 

  • Sanchez Marquez S, Bills GF, Dominguez Acuna L, Zabalgogeazcoa I (2010) Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Divers 41:115–123

    Article  Google Scholar 

  • Sanderson MA, Reed RL, McLaughlin SB, Wullschleger SD, Conger BV, Parrish DJ, Wolf DD, Taliaferro C, Hopkins AA, Ocumpaugh WR, Hussey MA, Read JC, Tischler CR (1996) Switchgrass as a sustainable bioenergy crop. Bioresour Technol 56:83–93

    Article  CAS  Google Scholar 

  • SAS (2004) PROC IML, 9.1.3 ed. SAS Institute Inc., Cary, North Carolina

  • Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seed borne fungal endophytes. Annu Rev Plant Biol 55:315–340

    Article  PubMed  CAS  Google Scholar 

  • Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light: Piriformospora indica—a revolutionary plant growth promoting fungus. Curr Sci 79:1548–1554

    Google Scholar 

  • Stovall ME, Clay K (1988) The effect of the fungus, Balansia cyperi on growth and reproduction of purple nutsedge, Cyperus rotundus. New Phytol 109:351–359

    Article  Google Scholar 

  • Sylvia DM, Williams SE (Eds) (1992) Vesicular-arbuscular mycorrhizae and environmental stress. American Society of Agronomy, Madison, Wisconsin

  • USDA (1985) Soil survey of Grant County, Oklahoma. United States Department of Agriculture and Soil Conservation Services, p 117

  • USDA (2007a) Supplement to the soil survey of Alfalfa County, Oklahoma. United States Department of Agriculture and Natural Resources Conservation Services, p 107

  • USDA (2007b) Supplement to the soil survey of the Kay County, Oklahoma. United States Department of Agriculture and Natural Resources Conservation Services, p 127

  • USDA (2008) Supplement to the soil survey of Osage County, Oklahoma. United Stated Department of Agriculture and Natural Resources Conservation Services, p 145

  • Vogel KP, Brejda JJ, Walters DT, Buxton DR (2002) Switchgrass biomass production in the Midwest USA: harvest and nitrogen management. Agron J 94:413–420

    Article  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (eds) (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Academic, New York

    Google Scholar 

  • Wicklow DT, Roth S, Deyrup ST, Gloer JB (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109:610–618

    Article  PubMed  CAS  Google Scholar 

  • Wirsel SGR, Leibinger W, Ernst M, Mendgen K (2001) Genetic diversity of fungi closely associated with common reed. New Phytol 149:589–598

    Article  CAS  Google Scholar 

  • Yang JD, Worley E, Wang MY, Lahner B, Salt DE, Saha M, Udvardi M (2009) Natural variation for nutrient use and remobilization efficiencies in switchgrass. Bioenerg Res 2:257–266

    Article  Google Scholar 

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Acknowledgements

This work was supported by a grant (award # 4000064018) to the Bioenergy Science Center (BESC) by the U.S. Department of Energy and managed by Paul Gilna. We are grateful to Eric Worley, Andy Hopkins, Myoung-Hwan Chi, Andrew Porter, Yi-Ching Lee, Ruchi Singh, Shaopei Zhang and Sumana Bhat for their help during sample collections and/or processing. Thanks are due to the staff of Genomic Core Facility, Scientific Computing Department and Greenhouse for rDNA sequencing, automation of blast searches and care of experimental plants, respectively. Our sincere thanks are due to Michael Udvardi, Marilyn Roossinck and Carolyn Young for the comments and suggestions during the preparation of this manuscript.

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Correspondence to Kelly D. Craven.

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Ghimire, S.R., Charlton, N.D., Bell, J.D. et al. Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Diversity 47, 19–27 (2011). https://doi.org/10.1007/s13225-010-0085-6

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