Microbial Ecology

, Volume 52, Issue 1, pp 104–113 | Cite as

Changes in Communities of Fusarium and Arbuscular Mycorrhizal Fungi as Related to Different Asparagus Cultural Factors

  • Etienne Yergeau
  • Vladimir Vujanovic
  • Marc St-ArnaudEmail author


Asparagus (Asparagus officinalis) is a high-value perennial vegetable crop that has shown a marked decline in productivity after many years of continuous harvesting. This decline is caused by an increase in both abiotic (autotoxicity, harvesting pressure) and biotic stresses [fungal infections, mainly Fusarium crown and root rot (FCRR)]. To gain insight into disease development and possible mitigation strategies, we studied the effects of harvesting, time in the growing season, and field age on FCRR development, Fusarium species composition, and arbuscular mycorrhizal fungi (AMF) communities in both a controlled field experiment and an ecological survey of commercial fields. In one experiment, a 3-year-old asparagus field was subdivided into plots that were harvested or not and sampled throughout the growing season to assess short-term dominant Fusarium species shifts. In addition, diseased and healthy asparagus plants sampled from six commercial fields in the same geographical region were used to assess Fusarium and AMF communities in relation to different parameters. Fusarium and AMF communities were described by using a polymerase chain reaction (PCR)–denaturing gradient gel electrophoresis (DGGE) approach, and results were analyzed by mainly correspondence analysis and canonical correspondence analysis. Results showed that dominant Fusarium taxa assemblages changed throughout the growing season. Harvested plots had significantly more FCRR symptomatic plants at the end of the growing season, but this effect was not related with any trend in Fusarium community structure. Sampling site and plant age significantly influenced AMF community structure, whereas only sampling site consistently influenced the Fusarium community. Diseased and healthy plants harbored similar Fusarium and AMF communities. Shifts in Fusarium community might not be responsible for different disease incidence because they are ubiquitous regardless of plant health status or harvesting regime. The different incidence noted might rather be related to plant physiology, antagonist microbial communities, or soil parameters.


Arbuscular Mycorrhizal Fungus Fusarium Fusarium Species Arbuscular Mycorrhizal Fungus Community Asymptomatic Plant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by an NSERC grant to M. St-Arnaud and a CORPAQ-PAR team grant. Financial assistance to E. Yergeau was provided by an FQRNT postgraduate scholarship. S. Daigle is thanked for multiple correspondence, frequency table analysis, and principal component analysis. We are also indebted to S. Roy, M. Cormier, and G. Champagne for letting us sample their fields and to D.W. Sommerville for help in the fieldwork. G.A. Kowalchuk is gratefully acknowledged for insightful comments on this manuscript.


  1. 1.
    Bateman, GL, Murray, G (2001) Seasonal variations in populations of Fusarium species in wheat-field soil. Appl Soil Ecol 18: 117–128CrossRefGoogle Scholar
  2. 2.
    Burgess, LW (1981) General ecology of the Fusaria. In: Nelson, PE, Toussoun, TA, Cook, RJ (Eds.) Fusarium: Diseases, Biology, and Taxonomy. The Pennsylvania State University Press, University Park, pp 225–235Google Scholar
  3. 3.
    Burrows, R, Pfleger, FL, Waters, LJ (1990) Growth of seedling asparagus inoculated with Glomus fasciculatum and phosphorus supplementation. HortScience 25: 519–521Google Scholar
  4. 4.
    Casgrain, P, Legendre, P (2001) The R package for multivariate and spatial analysis. Département de sciences biologiques, Université de MontréalGoogle Scholar
  5. 5.
    Chang, DCN (1985) Asparagus mycorrhizae: growth effect and structural changes. In: Lougheed, EC, Tiessen, H (Eds.) Sixth International Asparagus Symposium, University of Guelph, pp 307–316Google Scholar
  6. 6.
    Damicone, JP, Manning, WJ (1985) Frequency and pathogenicity of Fusarium spp. isolated from first-year asparagus grown from transplants. Plant Dis 69: 413–416Google Scholar
  7. 7.
    Dehne, HW (1982) Interaction between vesicular–arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72: 1115–1119Google Scholar
  8. 8.
    Elmer, WH (2001) Fusarium diseases of asparagus. In: Summerell, BA, Leslie, JF, Backhouse, D, Bryden, WL, Burgess, LW (Eds.) Fusarium: Paul E Nelson Memorial Symposium. APS Press, St-Paul, MN, pp 248–262Google Scholar
  9. 9.
    Elmer, WH (2002) Influence of formononetin and NaCl on mycorrhizal colonization and Fusarium crown and root rot of asparagus. Plant Dis 86: 1318–1324CrossRefGoogle Scholar
  10. 10.
    Elmer, WH, Johnson, DA, Mink, GI (1996) Epidemiology and management of the diseases causal to asparagus decline. Plant Dis 80: 117–125CrossRefGoogle Scholar
  11. 11.
    Elmer, WH, Summerell, BA, Burgess, LW, Backhouse, D, Abubaker, AA (1997) Fusarium species associated with asparagus crowns and soil in Australia and New Zealand. Australas Plant Pathol 26: 255–261CrossRefGoogle Scholar
  12. 12.
    Filion, M, St-Arnaud, M, Fortin, JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141: 525–533CrossRefGoogle Scholar
  13. 13.
    Fromin, N, Hamelin, J, Tarnawski, S, Roesti, D, Jourdain-Miserez, K, Forestier, N, Teyssier-Cuvelle, S, Gillet, F, Aragno, M, Rossi, P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4: 634–643PubMedCrossRefGoogle Scholar
  14. 14.
    Gilbertson, RL, Manning, WJ (1983) Contamination of asparagus flowers and fruit by airborne spores of Fusarium moniliforme. Plant Dis 67: 1003–1004CrossRefGoogle Scholar
  15. 15.
    Grogan, RG, Kimble, KA (1959) The association of Fusarium wilt with the asparagus decline and replant problem in California. Phytopathology 49: 122–125Google Scholar
  16. 16.
    Hamel, C, Vujanovic, V, Jeannotte, R, Nakano-Hylander, A, St-Arnaud, M (2005) Negative feedback on a perennial crop: Fusarium crown and root rot of asparagus is related to changes in soil microbial community structure. Plant Soil 268: 75–87CrossRefGoogle Scholar
  17. 17.
    Helgason, T, Daniell, TJ, Husband, R, Fitter, AH, Young, JPW (1998) Ploughing up the wood-wide web. Nature 394: 431CrossRefPubMedGoogle Scholar
  18. 18.
    Hussey, RB, Peterson, RL, Tiessen, H (1984) Interactions between vesicular–arbuscular mycorrhizal fungi and asparagus. Plant Soil 79: 403–416CrossRefGoogle Scholar
  19. 19.
    Johnson, NC, Copeland, PJ, Crookston, RK, Pfleger, FL (1992) Mycorrhizae: possible explanation for yield decline with continuous corn and soybean. Agron J 84: 387–390CrossRefGoogle Scholar
  20. 20.
    Kowalchuk, GA, De Souza, FA, van Veen, JA (2002) Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol Ecol 11: 571–581CrossRefPubMedGoogle Scholar
  21. 21.
    Lacy, ML (1979) Effects of chemicals on stand establishment and yields of asparagus. Plant Dis Rep 63: 612–616Google Scholar
  22. 22.
    LaMondia, JA, Elmer, WH (1989) Pathogenicity and vegetative compatibility among isolates of Fusarium oxysporum and F. moniliforme colonizing asparagus tissues. Can J Bot 67: 2420–2424Google Scholar
  23. 23.
    Legendre, P, Legendre, L (1998) Numerical Ecology. Elsevier, Amsterdam, 853pGoogle Scholar
  24. 24.
    Matsubara, Y, Kayukawa, Y, Fukui, H (2000) Temperature–stress tolerance of asparagus seedlings through symbiosis with arbuscular mycorrhizal fungus. J Jpn Soc Hortic Sci 69: 570–575Google Scholar
  25. 25.
    Matsubara, Y, Ohba, N, Fukui, H (2001) Effect of arbuscular mycorrhizal fungus infection on the incidence of Fusarium root rot in asparagus seedlings. J Jpn Soc Hortic Sci 70: 202–206CrossRefGoogle Scholar
  26. 26.
    O'Donnell, K, Kistler, HC, Cigelnik, E, Ploetz, RC (1998) Multiple evolutionary origins of the fungus causing Panama-disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci USA 95: 2044–2049CrossRefPubMedGoogle Scholar
  27. 27.
    Pedersen, CT, Safir, GR, Parent, S, Caron, M (1991) Growth of asparagus in a commercial peat mix containing vesicular–arbuscular mycorrhizal (VAM) fungi and the effects of applied phosphorus. Plant Soil 135: 75–82CrossRefGoogle Scholar
  28. 28.
    Sanders, DC (1985) Influence of extended harvest duration on carbohydrates accumulation and yield of established asparagus. In: Lougheed, EC, Tiessen, H (Eds.) Sixth International Asparagus Symposium, University of Guelph, pp 333–337Google Scholar
  29. 29.
    Schreuder, W, Lamprecht, SC, Marasas, WFO, Calitz, FJ (1995) Pathogenicity of three Fusarium species associated with asparagus decline in South Africa. Plant Dis 79: 177–181CrossRefGoogle Scholar
  30. 30.
    Shelton, DR, Lacy, ML (1980) Effect of harvest duration on yield and on depletion of storage carbohydrates in asparagus roots. J Am Soc Hortic Sci 105: 332–335Google Scholar
  31. 31.
    Simon, L, Lalonde, M, Bruns, TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular–arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58: 291–295PubMedGoogle Scholar
  32. 32.
    St-Arnaud, M, Hamel, C, Caron, M, Fortin, JA (1995) Endomycorhizes VA et sensibilité des plantes aux maladies: synthèse de la littérature et mécanismes d'interaction potentiels. In: Fortin, JA, Charest, C, Piché, Y (Eds.) La symbiose mycorhizienne: état des connaissances. Orbis Publishing, Frelighsburg, Quebec, Canada, pp 51–87Google Scholar
  33. 33.
    Takatori, FH, Stillman, J, Souther, FD (1970) Asparagus yields and plant vigor as influenced by time and duration of cutting. Calif Agric 24: 9–11Google Scholar
  34. 34.
    ter Braak, CJF, Šmilauer, P (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, 500pGoogle Scholar
  35. 35.
    Tessier, J-G (2003) La culture de l'asperge. Centre de référence en agriculture et agroalimentaire du Québec, Sainte-Foy, Quebec, Canada, 70pGoogle Scholar
  36. 36.
    von Wintzingerode, F, Gobel, UB, Stackebrandt, E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21: 213–229PubMedCrossRefGoogle Scholar
  37. 37.
    Vujanovic, V, Hamel, C, Yergeau, E, St-Arnaud, M (2006) Biodiversity and biogeography of Fusarium species from northeastern North American asparagus fields based on microbiological and molecular approaches. Microb Ecol 51: 242–255CrossRefPubMedGoogle Scholar
  38. 38.
    Wacker, TL, Safir, GR, Stephens, CT (1990) Mycorrhizal fungi in relation to asparagus growth and Fusarium wilt. Acta Hortic 271: 417–422Google Scholar
  39. 39.
    Wacker, TL, Safir, GR, Stephenson, SN (1990) Evidence for succession of mycorrhizal fungi in Michigan asparagus. Acta Hortic 271: 273–278Google Scholar
  40. 40.
    White, TJ, Bruns, TD, Lee, S, Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, MA, Gelfand, DH, Sninsky, JJ, White, TJ (Eds.) PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp 315–322Google Scholar
  41. 41.
    Yang, H (1982) Autotoxicity of Asparagus officinalis. J Am Soc Hortic Sci 107: 860–862Google Scholar
  42. 42.
    Yergeau, E, Filion, M, Vujanovic, V, St-Arnaud, M (2005) A PCR-denaturing gradient gel electrophoresis (DGGE) approach to assess Fusarium diversity in asparagus. J Microbiol Methods 60: 143–154CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Etienne Yergeau
    • 1
    • 2
  • Vladimir Vujanovic
    • 1
  • Marc St-Arnaud
    • 1
    Email author
  1. 1.Institut de recherche en biologie végétaleUniversité de Montréal and Jardin botanique de MontréalMontréalCanada
  2. 2.Department of Terrestrial Microbial EcologyNetherlands Institute of Ecology (NIOO-KNAW), Center for Terrestrial EcologyHeterenThe Netherlands

Personalised recommendations