Skip to main content
SpringerLink
Log in

Effects of a plant parasitic nematode (Heterodera trifolii) on clover roots and soil microbial communities

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

We studied the effects of the root endoparasitic nematode Heterodera trifolii on rhizodeposition and the root architecture of white clover (Trifolium repens). Rhizosphere solutions were collected from the root systems of plants growing with and without H. trifolii (200 juveniles per inoculated plant) in sand-based microlysimeters. The organic carbon (C) content of these solutions was analyzed, and they were applied to plant-free soils to investigate microbial responses. Although plant biomass was unaffected by nematodes, the architecture of the root systems was significantly altered, with a decrease in overall root length and an increase in the density of lateral branches from the primary root. The presence of nematodes reduced the concentration of organic compounds in the rhizosphere solutions but only on the final sampling date (75 days). Analysis of microbial signature phospholipid fatty acids revealed no change in the structure of the microbial communities in soils to which rhizosphere solutions were applied. However, these microorganisms did respond with changes in substrate utilization patterns (community-level physiological profiles). Microbes in soils that received rhizosphere solutions from the nematode-infected clover showed lower utilization of most substrates but higher utilization of oligosugars. These responses appear to be related to changes in roots and rhizodeposition associated with nematode infection of clover roots. The results of this study suggest that root herbivory can negatively impact carbon-limited soil microbial communities via changes in root architecture that moderate rhizodeposition.

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

Similar content being viewed by others

References

  • Alston DG, Schmitt DP (1988) Development of Heterodera glycines life stages as influenced by temperature. J Nematol 20:366–372

    CAS  PubMed  Google Scholar 

  • Bardgett RD, Cook R (1998) Functional aspects of soil animal diversity in agricultural grasslands. Appl Soil Ecol 10:263–276

    Article  Google Scholar 

  • Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268

    Google Scholar 

  • Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878

    Article  CAS  Google Scholar 

  • Bardgett RD, Cook R, Yeates GW, Denton CS (1999a) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33

    Article  CAS  Google Scholar 

  • Bardgett RD, Denton CS, Cook R (1999b) Below-ground herbivory promotes soil nutrient transfer and root growth in grassland. Ecol Lett 2:357–360

    Article  Google Scholar 

  • Berntson GM (1992) A computer-program for characterizing root system branching patterns. Plant Soil 140:145–149

    Article  Google Scholar 

  • Bostock RM, Stermer BA (1989) Perspectives on wound healing in resistance to pathogens. Annu Rev Phytopathol 27:343–371

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid and direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon sources in sole carbon utilization tests to discriminate soil microbial communities. J Microbiol Meth 30:33–41

    Article  Google Scholar 

  • Dawson LA, Grayston SJ, Murray PJ, Pratt SM (2002) Root feeding behavior of Tipula paludosa (Meig.) (Diptera: Tipulidae) on Lolium perenne (L.) and Trifolium repens (L.). Soil Biol Biochem 34:609–615

    Article  CAS  Google Scholar 

  • Dawson LA, Grayston SJ, Murray PJ, Cook R, Gange AC, Ross JM, Pratt SM, Duff EI, Treonis A (2003) Influence of pasture management (nitrogen and lime addition and insecticide treatment) on soil organisms and pasture root system dynamics in the field. Plant Soil 255:121–130

    Article  CAS  Google Scholar 

  • Denton CS, Badgett RD, Cook R, Hobbs PJ (1999) Low amounts of root herbivory positively influence the rhizosphere microbial community in a temperate grassland soil. Soil Biol Biochem 31:155–165

    Article  CAS  Google Scholar 

  • Federle TW (1986) Microbial distribution in the soil—new techniques. In: Megusar F, Gantar M (eds) Perspectives in microbial ecology. Slovene Society for Microbiology, Ljubljana, pp 493–498

    Google Scholar 

  • Ferris JM, Ferris VR (1998) Biology of plant-parasitic nematodes. In: Barker KR, Pederson GA, Windham GL (eds) Plant and nematode interactions. American Society of Agronomy, Madison, pp 21–35

    Google Scholar 

  • Garland JL (1996) Analytical approaches to the characterisation of samples of microbial communities using patterns of potential C source utilisation. Soil Biol Biochem 28:213–221

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterisation of heterotrophic microbial communities on the basis of patterns of community-level-sole-carbon-source utilisation. Appl Environ Microbiol 57:2351–2359

    PubMed  CAS  Google Scholar 

  • Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56

    Article  Google Scholar 

  • Grayston SJ, Dawson LA, Treonis AM, Murray PH, Ross J, Reid EJ, MacDougall R (2001a) Impact of root herbivory by insect larvae on soil microbial communities. Eur J Soil Biol 37:277–280

    Article  CAS  Google Scholar 

  • Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001b) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551

    Article  CAS  Google Scholar 

  • Ingham RE, Detling JK (1990) Effects of root-feeding nematodes on aboveground net primary production in a North American grassland. Plant Soil 121:279–281

    Article  Google Scholar 

  • Jenkinson DS, Ladd JN (1981) Microbial biomass in soil-measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 415–471

    Google Scholar 

  • Moore JC, McCann K, Setala H, de Ruiter PC (2003) Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857

    Google Scholar 

  • Murray PJ, Hatch DJ, Cliquet JB (1996) Impact of insect root herbivory on the growth and nitrogen and carbon contents of white clover (Trifolium repens) seedlings. Can J Bot 74:1591–1595

    Google Scholar 

  • Nannipieri P, Ascher J, Cecccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Pederson GA, Quesenberry KH (1998) Clovers and other forage legumes. In: Barker KR, Pederson GA, Windham GL (eds) Plant and nematode interactions. American Society of Agronomy, Madison, pp 399–425

    Google Scholar 

  • Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894

    Article  PubMed  CAS  Google Scholar 

  • Thornton B, Millard P, Galloway S (1993) The effects of temperature and form of nitrogen supply on the relative contribution of root uptake and remobilisation in supplying nitrogen for laminae regrowth of Lolium perenne L. J Exp Bot 44:1601–1606

    Article  CAS  Google Scholar 

  • Treonis AM, Grayston SJ, Murray PJ, 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 

  • Tu C, Koenning SR, Hu S (2003) Root-parasitic nematodes enhance soil microbial activities and nitrogen mineralization. Microbial Ecol 46:134–144

    Article  CAS  Google Scholar 

  • Van der Putten WH, Anderson JM, Bardgett RD, Behan-Pelletier V, Bignell DE, Brown GG, Brown VK, Brussard L, Hunt HW, Ineson P, Jones TH, Lavelle P, Paul EA, St. John M, Wardle DA, Wojtowicz T, Wall DH (2004) The sustainable delivery of good and services provided by soil biota. In: DH Wall (ed) Sustaining biodiversity and ecosystem services in soils and sediments. Island, Washington, pp 15–43

    Google Scholar 

  • VanHecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:99–107

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • Yeates GW, Saggar S, Denton CD, Mercer CF (1998) Impact of clover cyst nematode (Heterodera trifolii) infection on soil microbial activity in the rhizosphere of white clover (Trifolium repens)—a pulse-labelling experiment. Nematologica 44:81–90

    Article  Google Scholar 

  • Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Karen Lowes, Brian Ord, Eileen Reid, Ruth Primrose, Jasmine Ross, and Allan Sim for assistance with this experiment. Two anonymous referees are thanked for their review of this manuscript. This research was funded by the Scottish Executive Environment and Rural Affairs Department (SERAD) and the UK’s Natural Environmental Research Council (NERC), and is a contribution to the NERC Soil Biodiversity Thematic Programme. The Institute for Grassland and Environmental Research (IGER) is supported by the Biotechnology and Biological Sciences Research Council (BBSRC).

Author information

Author notes

  1. Amy M. Treonis

    Present address: Department of Biology, University of Richmond, 28 Westhampton Way, Richmond, VA, 23173, USA

  2. Susan J. Grayston

    Present address: Department of Forest Sciences, University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada , V6T 1Z4

Authors and Affiliations

  1. The Macaulay Institute, Craigiebuckler, Aberdeen, AB24 3NJ, UK

    Amy M. Treonis, Lorna Dawson & Susan J. Grayston

  2. Institute for Grassland and Environmental Research, Aberystwyth Research Station, Aberystwyth, SY23 3EB, UK

    Roger Cook & Tony Mizen

Authors
  1. Amy M. Treonis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roger Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorna Dawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susan J. Grayston
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tony Mizen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amy M. Treonis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Treonis, A.M., Cook, R., Dawson, L. et al. Effects of a plant parasitic nematode (Heterodera trifolii) on clover roots and soil microbial communities. Biol Fertil Soils 43, 541–548 (2007). https://doi.org/10.1007/s00374-006-0133-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-006-0133-2

Keywords

Search

Navigation