Skip to main content
SpringerLink
Log in

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

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abelson PH (1999) A potential phosphate crisis. Science 238:2015

    Article  Google Scholar 

  • 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):1024–1039

    Article  CAS  PubMed  Google Scholar 

  • 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 155–178

    Google Scholar 

  • 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 23–26

  • Bertrand I, Holloway RE, Armstrong RD, McLaughlin MJ (2003) Chemical characteristics of phosphorus in alkaline soils from southern Australia. Aust J Soil Res Sci 41:61–76

    Article  CAS  Google Scholar 

  • Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Appl Soil Ecol 61:127–130

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 24:633–637

    Article  Google Scholar 

  • 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 64:197–214

    Article  CAS  Google Scholar 

  • 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 11:1355–1362

    Article  CAS  Google Scholar 

  • 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 107:662–670

    Article  CAS  Google Scholar 

  • 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 42:243–270

    Article  CAS  PubMed  Google Scholar 

  • 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 46:71–79

    Article  Google Scholar 

  • Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378

    Article  CAS  Google Scholar 

  • 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 84:882–885

    Article  Google Scholar 

  • 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 6:1–13

    Google Scholar 

  • 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 48:151–159

    Article  Google Scholar 

  • 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 57:625–634

    Article  CAS  Google Scholar 

  • 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 46:970–976

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. J Appl Ecol 42:762–769

    Article  Google Scholar 

  • 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 46:79–91

    Article  CAS  Google Scholar 

  • 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:e48010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 51–81

    Google Scholar 

  • Mack KM, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320

    Article  Google Scholar 

  • Maher FM, Thorrold BS (1989) Accumulation of phosphorus fractions in yellow-brown pumice soils with development. N Z J Agric Res 32:53–62

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 205:1–12

    Article  CAS  Google Scholar 

  • 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 198:53–61

    Article  CAS  Google Scholar 

  • Malinowski DP, Brauer DK, Belesky DP (1999) Neotyphodium coenophiadium-endophyte affects root morphology of tall fescue grown under phosphorus deficiency. J Agron Crop Sci 183:53–60

    Article  CAS  Google Scholar 

  • 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 28:194–204

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • 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 65:359–367

    Article  CAS  Google Scholar 

  • Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rechcigl JE, Payne GG (1990) Comparison of a microwave digestion system to other digestion methods for plant tissue analysis. Commun Soil Sci Plant Anal 21:2209–2218

    Article  CAS  Google Scholar 

  • 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 321:305–339

    Article  CAS  Google Scholar 

  • 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 349:121–156

    Article  CAS  Google Scholar 

  • Rudgers JA, Fischer S, Clay K (2010) Managing plant symbiosis: fungal endophyte genotype alters plant community composition. J Appl Ecol 47:48–477

    Article  Google Scholar 

  • 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 34:1309–1315

    Article  CAS  Google Scholar 

  • Sinsabaugh RL (1994) Enzymic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74

    Article  CAS  Google Scholar 

  • 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 43:565–574

    Article  CAS  Google Scholar 

  • Tadano T, Sakai H (1991) Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions. Soil Sci Plant Nutr 37:129–140

    Article  CAS  Google Scholar 

  • 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):95–98

    Article  Google Scholar 

  • Tawaraya K, Naito M, Wagatsuma T (2006) Solubilization of insoluble inorganic phosphate by hyphal exudates of arbuscular mycorrhizal fungi. J Plant Nutr 29:657–665

    Article  CAS  Google Scholar 

  • 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 28:203–215

    Article  Google Scholar 

  • U.S. Environmental Protection Agency (1971) Methods of chemical analysis for water and wastes. Cincinnati, OH, USA

  • 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

    Article  CAS  Google Scholar 

  • 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 348:85–98

    Article  CAS  Google Scholar 

  • 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 248:128–136

    Article  Google Scholar 

  • 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 18:1235–1252

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Author notes

  1. Haichao Guo

    Present address: Horticultural Sciences Department, University of Florida, Gainesville, FL, USA

Authors and Affiliations

  1. Rhizosphere Science Laboratory, Department of Plant and Soil Science, University of Kentucky, Lexington, KY, USA

    Na Ding, Haichao Guo, Joseph V. Kupper & David H. McNear Jr.

Authors
  1. Na Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haichao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph V. Kupper
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David H. McNear Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Na Ding.

Additional information

Responsible Editor: Peter Christie .

Electronic supplementary material

Below is the link to the electronic supplementary material.

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)

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)

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)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, N., Guo, H., Kupper, J.V. et al. Shoot specific fungal endophytes alter soil phosphorus (P) fractions and potential acid phosphatase activity but do not increase P uptake in tall fescue. Plant Soil 401, 291–305 (2016). https://doi.org/10.1007/s11104-015-2757-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2757-1

Keywords

Search

Navigation