Plant and Soil

, Volume 401, Issue 1–2, pp 291–305 | Cite as

Shoot specific fungal endophytes alter soil phosphorus (P) fractions and potential acid phosphatase activity but do not increase P uptake in tall fescue

  • Na Ding
  • Haichao Guo
  • Joseph V. Kupper
  • David H. McNearJr.
Regular Article



An experiment was performed to test how different fungal endophyte strains influenced tall fescue’s ability to access P from four P sources varying in solubility.


Novel endophyte infected (AR542E+ or AR584E+), common toxic endophyte infected (CTE+), or endophyte-free (E-) tall fescues were grown for 90 days in acidic soils amended with 30 mg kg−1 P of potassium dihydrogen phosphate (KH2PO4), iron phosphate (FePO4), aluminum phosphate (AlPO4), or tricalcium phosphate ((Ca3(PO4)2), respectively.


Phosphorus form strongly influenced plant biomass, P acquisition, agronomic P use efficiency, microbial communities, P fractions. P uptake and vegetative biomass were similar for plants grown with AlPO4, Ca3(PO4)2, and KH2PO4 but greater than in control and FePO4 soils. Infection with AR542E+ resulted in significantly less shoot biomass than CTE+ and E- varieties; there was no influence of endophyte on root biomass. The biomarker for arbuscular mycorrhizal fungi (AM fungi, 16:1ω5c) was selected as an effective predictor of variations in P uptake and tall fescue biomass. Potential acid phosphatase activity was strongly influenced by endophyte x P form interaction.


Endophyte infection in tall fescue significantly affected the NaOH-extractable inorganic P fraction, but had little detectable influence on soil microbial community structure, root biomass, or P uptake.


Neotyphodium coenophialum Epichloë coenophiala Microbial community Phospholipid fatty acids (PLFAs) Phosphorus fractions Potential acid phosphatase activity (AcPase) 



We thank Dr. Mark S. Coyne for helpful comments on this manuscript. We also thank collaborators at the Noble Foundation for providing the seed gifts. This work was financially supported by National Research Initiative no. 2011-67019-30392 from the USDA National Institute of Food and Agriculture.

Supplementary material

11104_2015_2757_MOESM1_ESM.docx (30 kb)
Fig. S1 The influence of endophyte x P form interaction on P concentrations in root tissues. Means not sharing the same letter are significantly different (p < 0.05), Bar represents ± the standard error of the mean. (DOCX 30 kb)
11104_2015_2757_MOESM2_ESM.docx (99 kb)
Fig. S2 Two-dimensional solution of nonmetric multidimensional scaling (NMS) plot using the relative abundance of PLFA biomarker groups in rhizosphere soils under tall fescue (E-, CTE+, AR542E+ and AR584E+) from the control (No-P) treatment and those receiving treatment with four P sources [(a) K-Ps, (b) Fe-Ps, (c) Al-Ps, (d) Ca-Ps], individually. Radiating lines from the ordination centroid indicate the strength and direction of Pearson correlations (r2 > 0.4) between variables and stand axis scores. Actino = actinobacteria, EU = eukaryote, TMB = total microbial biomass (DOCX 99 kb)
11104_2015_2757_MOESM3_ESM.docx (13 kb)
Table S1 Concentration of PLFA biomarker groups and total microbial biomass (TMB; nmol•g-1 soil) in pre-planted (14 days after P addition before planting tall fescue), and rhizosphere soils after 90-days of tall fescue growth in control soils and those receiving 30 mg•kg-1 of four P forms (K-Ps, Fe-Ps, Al-Ps, Ca-Ps). Results from linear contrasts comparing microbial parameters in rhizosphere vs. pre-planted soils appear in the bottom portion of the table. (DOCX 13 kb)


  1. Abelson PH (1999) A potential phosphate crisis. Science 238:2015CrossRefGoogle Scholar
  2. Akhtar MS, Oki Y, Adachi T (2009) Mobilization and acquisition of sparingly soluble P-sources by Brassica cultivars under P-starved environmental. II. Rhizospheric pH changes, redesigned root architecture and Pi-uptake kinetics. J Integr Plant Biol 51(11):1024–1039CrossRefPubMedGoogle Scholar
  3. Bacon CW, Hill NS (1996) Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaption of infected grasses. In: Redlin SC, Carris LM (eds) Systematics, ecology and evolution of endophytic fungi of grasses and woody plants. American Phytopathological Society Press, St. Paul, pp 155–178Google Scholar
  4. Belesky DP, Burner DM (2004) Germination and seedling development of a tall fescue cultivar in response to native and novel endophyte. In: Kallenbach R, Rosenkrans C Jr, Lock TR (eds) Proceedings of the 5th International Symposium o Neotyphodium/Grass Interactions. Fayetteville, pp 23–26Google Scholar
  5. Bertrand I, Holloway RE, Armstrong RD, McLaughlin MJ (2003) Chemical characteristics of phosphorus in alkaline soils from southern Australia. Aust J Soil Res Sci 41:61–76CrossRefGoogle Scholar
  6. Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Appl Soil Ecol 61:127–130CrossRefGoogle Scholar
  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 339:401–412CrossRefGoogle Scholar
  8. Chu-Chou M, Guo B, An ZQ, Hendrix JW, Ferriss RS, Siegel MR, Burrus PB (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24:633–637CrossRefGoogle Scholar
  9. Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214CrossRefGoogle Scholar
  10. Ding N, Tahir H, Wang J, Wang HZ, Liu XM, Xu JM (2011) Responses of microbial community in rhizosphere soils when ryegrass was subjected to stress from PCBs. J Soils Sediments 11:1355–1362CrossRefGoogle Scholar
  11. Ding N, Kupper VJ, McNear HM (2015) Phosphate source interacts with endophyte strain to influence biomass and root system architecture in tall fescue. Agron J 107:662–670CrossRefGoogle Scholar
  12. Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implication on disease suppressiveness. Annu Rev Phytopathol 42:243–270CrossRefPubMedGoogle Scholar
  13. Ghosh GK, Mohan KS, Sarkar AK (1996) Characterization of soil-fertilizer P reaction products and their evaluation as sources of P for gram (Cicer arietinum L.). Nutr Cycl Agroecosyst 46:71–79CrossRefGoogle Scholar
  14. Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  15. Guo BZ, Hendrix JW, An Z-Q, Ferriss RS (1992) Role of Acremonium endophyte of fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 84:882–885CrossRefGoogle Scholar
  16. Guo J, McCulley RL, McNear DH Jr (2015) Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Front Plant Sci 6:1–13Google Scholar
  17. Hassan HM, Marschner P, McNeill A, Tang C (2012) Growth, P uptake in grain legumes and changes in rhizosphere soil P pools. Biol Fertil Soils 48:151–159CrossRefGoogle Scholar
  18. He Y, Ding N, Shi JC, Wu M, Liao H, Xu JM (2013) Profiling of microbial PLFAs: implications for interspecific interactions due to intercropping which increase phosphorus uptake in phosphorus limited acidic soils. Soil Biol Biochem 57:625–634CrossRefGoogle Scholar
  19. Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976CrossRefGoogle Scholar
  20. Hiatt EE, Hill NS, Bouton JH, Stuedemann JA (1999) Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Sci 39:796–799CrossRefGoogle Scholar
  21. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  22. Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. J Appl Ecol 42:762–769CrossRefGoogle Scholar
  23. Li HG, Shen JB, Zhang FS, Marschner P, Cawthray G, Rengel Z (2010) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biol Fertil Soils 46:79–91CrossRefGoogle Scholar
  24. Li X, Ren A, Han R, Yin L, Wei M, Gao Y (2012) Endophyte-mediated effects on the growth and physiology of Achnatherum sibiricum are conditional on both N and P availability. PLoS ONE 7:e48010CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lynch JP, Brown MK (2008) Root strategies for phosphorus acquisition. In: White PJ, Hammond JP (eds) The Ecophysiology of plant-phosphorus interactions. Springer, Netherlands, pp 51–81Google Scholar
  26. Mack KM, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320CrossRefGoogle Scholar
  27. Maher FM, Thorrold BS (1989) Accumulation of phosphorus fractions in yellow-brown pumice soils with development. N Z J Agric Res 32:53–62CrossRefGoogle Scholar
  28. Malinowski DP, Belesky DP (2000) Adaptations of Endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  29. Malinowski DP, Alloush GA, Belesky DP (1998a) Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 205:1–12CrossRefGoogle Scholar
  30. Malinowski DP, Belesky DP, Hill NS, Baligar VC, Fedders JM (1998b) Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb). Plant Soil 198:53–61CrossRefGoogle Scholar
  31. Malinowski DP, Brauer DK, Belesky DP (1999) Neotyphodium coenophiadium-endophyte affects root morphology of tall fescue grown under phosphorus deficiency. J Agron Crop Sci 183:53–60CrossRefGoogle Scholar
  32. Marks S, Clay K, Cheplick GP (1991) Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. J Appl Ecol 28:194–204CrossRefGoogle Scholar
  33. Murphy J, Riley JP (1962) A modified single solution for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  34. Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367CrossRefGoogle Scholar
  35. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rechcigl JE, Payne GG (1990) Comparison of a microwave digestion system to other digestion methods for plant tissue analysis. Commun Soil Sci Plant Anal 21:2209–2218CrossRefGoogle Scholar
  37. Richardson AE, Barea J, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339CrossRefGoogle Scholar
  38. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith A, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156CrossRefGoogle Scholar
  39. Rudgers JA, Fischer S, Clay K (2010) Managing plant symbiosis: fungal endophyte genotype alters plant community composition. J Appl Ecol 47:48–477CrossRefGoogle Scholar
  40. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term deposition on extracellular enzyme activity in an Acer saccarum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  41. Sinsabaugh RL (1994) Enzymic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74CrossRefGoogle Scholar
  42. Song YN, Zhang FS, Marschner P, Fan FL, Gao HM, Bao XG, Sun JH, Li L (2007) Effect of intercropping on crop yield and chemical and microbiological properties in rhizosphere of wheat (Triticum aestivum L.), maize (Zea mays L.), and faba bean (Vicia faba L.). Biol Fertil Soils 43:565–574CrossRefGoogle Scholar
  43. Tadano T, Sakai H (1991) Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions. Soil Sci Plant Nutr 37:129–140CrossRefGoogle Scholar
  44. Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil 155(156):95–98CrossRefGoogle Scholar
  45. Tawaraya K, Naito M, Wagatsuma T (2006) Solubilization of insoluble inorganic phosphate by hyphal exudates of arbuscular mycorrhizal fungi. J Plant Nutr 29:657–665CrossRefGoogle Scholar
  46. Treonis AM, Grayston SJ, Murray PH, Dawson LA (2005) Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Appl Soil Ecol 28:203–215CrossRefGoogle Scholar
  47. U.S. Environmental Protection Agency (1971) Methods of chemical analysis for water and wastes. Cincinnati, OH, USAGoogle Scholar
  48. 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 275:101–109CrossRefGoogle Scholar
  49. Wang X, Guppy CN, Watson L, Sale PWG, Tang C (2011) Availability of sparingly soluble phosphorus sources to cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.) and white lupin (Lupinus albus L.) by a 32P isotopic dilution technique. Plant Soil 348:85–98CrossRefGoogle Scholar
  50. Wasaki J, Yamamura T, Shinana T, Osaki M (2003) Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant Soil 248:128–136CrossRefGoogle Scholar
  51. Wright RJ, Baligar VC, Wright SF (1987) The influence of acid soil factors on the growth of snapbeans in major Appalachian soils. Commun Soil Sci Plant Anal 18:1235–1252CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Na Ding
    • 1
  • Haichao Guo
    • 1
    • 2
  • Joseph V. Kupper
    • 1
  • David H. McNearJr.
    • 1
  1. 1.Rhizosphere Science Laboratory, Department of Plant and Soil ScienceUniversity of KentuckyLexingtonUSA
  2. 2.Horticultural Sciences DepartmentUniversity of FloridaGainesvilleUSA

Personalised recommendations