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Negative feedback on a perennial crop: Fusarium crown and root rot of asparagus is related to changes in soil microbial community structure

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Abstract

The dynamic equilibrium of an ecosystem is driven by mutual feedback interactions between plants and soil microorganisms. Asparagus exerts a particularly strong influence on its soil environment through abundant production of persistent phenolic acids, which impact selectively soil microorganisms and may be involved in Fusarium crown and root rot (FCRR) of asparagus. In a survey of 50 asparagus plantations of the province of Québec, we found that FCRR was associated with a profound cultivar-specific, reorganization of the soil microbial community, as revealed by phospholipid fatty acid (PLFA) profiling. According to PLFA indicators, microbial biodiversity as well as bacterial and fungal abundance dropped sharply with the onset of FCRR in fields planted with the cultivar Guelph Millenium. This drop was followed by a similar drop in the arbuscular mycorrhizal population. Biodiversity and microbial population size then increased to finally reach a new equilibrium. Discriminant analysis of PLFA profiles obtained from soil samples also indicated a shift in soil microbial community structure associated with FCRR development in fields planted with the cultivar Jersey Giant. Different soil biological conditions, as indicated by microbial biomass C and N and soil enzyme activities, were associated with different cultivars. Preceding crop, manure application, geographical location and tillage depth also influenced the structure of soil microbial communities in asparagus plantations, as determined by PLFA profiling. If higher FCRR incidence is a consequence of the soil microbial community reorganization, means to reduce FCRR incidence in asparagus plantations may be found among practices such as soil organic fertilization, soil tillage and intercropping strategies that would dilute the negative influence of asparagus on the soil microbial community. Finally, FCRR outbreaks were generally promoted by a previous crop of maize. It seems that maize and asparagus host a F. proliferatum teleomorph (Gibberella fujikoroi) of the same mating type.

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Abbreviations

FCRR:

Fusarium crown and root rot

PLFA:

phospholipid fatty acid

FAME:

fatty acid methyl ester

References

  • R P Baayen P Boogert Particlevan den P J M Bonants J T K Poll W J Blok C Waalwijk (2000) ArticleTitleFusarium redolens f.sp asparagi, causal agent of asparagus root rot, crown rot and spear rot Eur. J. Plant Pathol 106 907–912

    Google Scholar 

  • R D Bardgett R D Lovell P J Hobbs S C Jarvis (1999) ArticleTitleSeasonal changes in soil microbial communities along a fertility gradient of temperate grasslands Soil Biol. Biochem 31 1021–1030 Occurrence Handle1:CAS:528:DyaK1MXjsFCnu7w%3D

    CAS  Google Scholar 

  • J D Bever (2003) ArticleTitleSoil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests New Phytol 157 465–473

    Google Scholar 

  • J D Bever K M Westover J Antonovics (1997) ArticleTitleIncorporating the soil community into plant population dynamics: The utility of the feedback approach J. Ecol 85 561–573

    Google Scholar 

  • A C Bily L M Reid J H Taylor D Johnston C Malouin A J Burt B Bakan C Regnault-Roger K P Pauls J T Arnason B J R Philogene (2003) ArticleTitleDehydrodimers of ferulic acid in maize grain pericarp and aleurone: Resistance factors to Fusarium graminearum Phytopathology 93 712–719 Occurrence Handle1:CAS:528:DC%2BD3sXkslKmu7s%3D

    CAS  Google Scholar 

  • W J Blok M J Zwankhuizen G J Bollen (1997) ArticleTitleBiological control of Fusarium oxysporum f.sp.asparagi by applying non-pathogenic isolates of F. oxysporum Biocontrol Sci. Technol 7 527–541

    Google Scholar 

  • W J Blok G J Bollen (1996a) ArticleTitleEtiology of asparagus replant bound early decline Eur. J. Plant Pathol 102 87–98

    Google Scholar 

  • W J Blok G J Bollen (1996b) ArticleTitleInoculum sources of Fusarium oxysporum f.sp.asparagi in asparagus production Ann. Appl. Biol 128 219–231

    Google Scholar 

  • W J Blok G J Bollen (1996c) ArticleTitleInteractions of asparagus root tissue with soil microorganisms as a factor in early decline of asparagus Plant Pathol 45 809–822

    Google Scholar 

  • D A Bossio K M Scow N Gunapala K J Graham (1998) ArticleTitleDeterminants of soil microbial communities: effects of agricultural management, season and soil type on phospholipid fatty acid profiles Microb. Ecol 36 1–12 Occurrence Handle1:CAS:528:DyaK1cXksVOrt78%3D Occurrence Handle9622559

    CAS  PubMed  Google Scholar 

  • L W Burgess C M Liddell B A Summerell (1988) Laboratory Manual for Fusarium Research University of Sydney Sydney

    Google Scholar 

  • S N Chulze M L Ramirez A Torres J F Leslie (2000) ArticleTitleGenetic variation in Fusarium section Liseola from no-till maize in Argentina Appl. Environ. Microbiol 66 5312–5315 Occurrence Handle1:STN:280:DC%2BD3M7itVOmsA%3D%3D Occurrence Handle11097907

    CAS  PubMed  Google Scholar 

  • A Ascensao Particlede I A Dubery (2003) ArticleTitleSoluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp cubense Phytochemistry 63 679–686 Occurrence Handle12842140

    PubMed  Google Scholar 

  • H W Dehne (1982) ArticleTitleInteraction between vesicular-arbuscular mycorrhizal fungi and plant pathogens Phytopathology 72 1115–1119

    Google Scholar 

  • C El Modafar E El Boustani (2001) ArticleTitleCell wall-bound phenolic acid and lignin contents in date palm as related to its resistance to Fusarium oxysporum Biol. Plant 44 125–130 Occurrence Handle1:CAS:528:DC%2BD3MXjtFygsL4%3D

    CAS  Google Scholar 

  • C El Modafar E El Boustani (2000) ArticleTitleRelationship between cell wall susceptibility to cellulases and pectinases of Fusarium oxysporumand susceptibility of date palm cultivars Biol. Plant 43 571–576 Occurrence Handle1:CAS:528:DC%2BD3cXosFKisro%3D

    CAS  Google Scholar 

  • W H Elmer (1995a) ArticleTitleAssociation between Mn-reducing root bacteria and NaCl applications in suppression of Fusarium crown and root rot of asparagus Phytopathology 85 1461–1467

    Google Scholar 

  • W H Elmer (1995b) ArticleTitleA single mating population of Gibberella fujikuroi (Fusarium proliferatum) predominates in asparagus fields in Connecticut, Massachusetts, and Michigan Mycologia 87 68–71

    Google Scholar 

  • W H Elmer (1996) ArticleTitleEpidemiology and management of the diseases causal to asparagus decline Plant Dis 80 117–125

    Google Scholar 

  • W H Elmer (2000) ArticleTitleIncidence of infection of asparagus spears marketed in Connecticut by Fusarium spp Plant Dis 84 831–834

    Google Scholar 

  • W H Elmer (2001) Fusarium diseases of asparagus B A Summerell J F Leslie D Backhouse W L Bryden L W Burgess (Eds) Fusarium: Paul E.Nelson Memorial Symposium APS Press St. Paul 248–262

    Google Scholar 

  • W H Elmer (2002) ArticleTitleInfluence of formononetin and NaCl on mycorrhizal colonization and Fusarium crown and root rot of asparagus Plant Dis 86 1318–1324 Occurrence Handle1:CAS:528:DC%2BD38XpsFSit78%3D

    CAS  Google Scholar 

  • W H Elmer (2003) ArticleTitleLocal and systemic effects of NaCl on root composition, rhizobacteria, and Fusarium crown and root rot of asparagus Phytopathology 93 186–192

    Google Scholar 

  • W H Elmer J A LaMondia B Benson (1999) ArticleTitleStudies on the supression of Fusarium crown and root rot of asparagus with NaCl Acta Hort 479 211–217 Occurrence Handle1:CAS:528:DyaK1MXjtFGjtrc%3D

    CAS  Google Scholar 

  • A H Eom D C Hartnett G W T Wilson (2000) ArticleTitleHost plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie Oecologia 122 435–444

    Google Scholar 

  • C W Fang M Radosevich J J Fuhrmann (2001) ArticleTitleCharacterization of rhizosphere microbial community structure in five similar grass species using FAME and BIOLOG analyses Soil Biol. Biochem 33 679–682 Occurrence Handle1:CAS:528:DC%2BD3MXis1aksLY%3D

    CAS  Google Scholar 

  • D Fravel C Olivain C Alabouvette (2003) ArticleTitleFusarium oxysporum and its biocontrol New Phytol 157 493–502

    Google Scholar 

  • A Frostegard E Baath (1996) ArticleTitleThe use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil Biol. Fertil. Soils 22 59–65

    Google Scholar 

  • W Gerlach H Nirenberg (1982) The Genus Fusarium – A Pictorial Atlas Verlag Paul Parey Berlin 406

    Google Scholar 

  • M Giovannetti B Mosse (1980) ArticleTitleAn evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots New Phytol 84 489–500

    Google Scholar 

  • S J Grayston G S Griffith J L Mawdley C D Campbell R D Bardgett (2001) ArticleTitleAccounting for variability in soil microbial communities of temperate upland grassland ecosystems Soil Biol. Biochem 33 533–551 Occurrence Handle1:CAS:528:DC%2BD3MXis1aks70%3D

    CAS  Google Scholar 

  • K Hedlund (2002) ArticleTitleSoil microbial community structure in relation to vegetation management on former agricultural land Soil Biol. Biochem 34 1299–1307 Occurrence Handle1:CAS:528:DC%2BD38XlvVemu78%3D

    CAS  Google Scholar 

  • N C Johnson P J Copeland R K Crookston F L Pfleger (1992) ArticleTitleMycorrhizae: Possible explanation for yield decline with continuous corn and soybean Agron. J 84 387–390

    Google Scholar 

  • J N Klironomos (2002) ArticleTitleFeedback with soil biota contributes to plant rarity and invasiveness in communities Nature 417 67–70 Occurrence Handle1:CAS:528:DC%2BD38XjsFOgtbo%3D Occurrence Handle11986666

    CAS  PubMed  Google Scholar 

  • R J Lake P G Falloon D W M Cook (1993) ArticleTitleReplant problem and chemical components of asparagus roots New Zealand J. Crop Horicult. Sci 21 53–58 Occurrence Handle1:CAS:528:DyaK3sXlsl2qtrg%3D

    CAS  Google Scholar 

  • J F Leslie (1991) ArticleTitleMating populations of Gibberella fujikuroi (Fusarium Section Liseola) Phytopathology 81 1058–1060

    Google Scholar 

  • S J Macnaughton T L Jenkins M H Wimpee M R Cormier D C White (1997) ArticleTitleRapid extraction of lipid biomarkers from pure culture and environmental samples using pressurized accelerated hot solvent extraction J. Microbiol. Methods 31 19–27 Occurrence Handle1:CAS:528:DyaK2sXnvVWjsLk%3D

    CAS  Google Scholar 

  • Y Matsubara N Hasegawa H Fukui (2002) ArticleTitleIncidence of Fusarium root rot in asparagus seedlings infected with arbuscular mycorrhizal fungus as affected by several soil amendments J. Jpn. Soc. Hortic. Sci 71 370–374

    Google Scholar 

  • Y Matsubara N Ohba H Fukui (2001) ArticleTitleEffect of arbuscular mycorrhizal fungus infection on the incidence of Fusarium root rot in asparagus seedlings J. Jpn. Soc. Hortic. Sci 70 202–206

    Google Scholar 

  • G P Munkvold J K O’Mara (2002) ArticleTitleLaboratory and growth chamber evaluation of fungicidal seed treatments for maize seedling blight caused by Fusarium species Plant Dis 86 143–150 Occurrence Handle1:CAS:528:DC%2BD38XhtVCmurc%3D

    CAS  Google Scholar 

  • P E Nelson T A Toussoun W F O Marasas (1983) Fusarium Species: An Illustrated Manual for Identification The Pennsylvania State University Press University Park 193

    Google Scholar 

  • P A Olsson (1999) ArticleTitleSignature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil FEMS Microbiol. Ecol 29 303–310 Occurrence Handle1:CAS:528:DyaK1MXls1anu74%3D

    CAS  Google Scholar 

  • M Ongena F Daayf P Jacques P Thonart N Benhamou T C Paulitz R R Belanger (2000) ArticleTitleSystemic induction of phytoalexins in cucumber in response to treatments with fluorescent pseudomonads Plant Pathol 49 523–530 Occurrence Handle10.1046/j.1365-3059.2000.00468.x Occurrence Handle1:CAS:528:DC%2BD3cXmtFOmsbs%3D

    Article  CAS  Google Scholar 

  • C E Pankhurst A Pierret B G Hawke J M Kirby (2002) ArticleTitleMicrobiological and chemical properties of soil associated with macropores at different depths in a red-duplex soil in NSW Australia Plant Soil 238 11–20 Occurrence Handle1:CAS:528:DC%2BD38Xit1Grurk%3D

    CAS  Google Scholar 

  • C T Pederson G R Safir J O Siqueira S Parent (1991) ArticleTitleEffect of phenolic compounds on asparagus mycorrhiza Soil Biol. Biochem 23 491–494

    Google Scholar 

  • R D Reeleder (2003) ArticleTitleFungal plant pathogens and soil biodiversity Can. J. Soil Sci 83 331–336

    Google Scholar 

  • T C Reid M K Hausbeck K Kizilkaya (2002) ArticleTitleUse of Fungicides and biological controls in the suppression of Fusarium crown and root rot of asparagus under greenhouse and growth chamber conditions Plant Dis 86 493–498 Occurrence Handle1:CAS:528:DC%2BD38XjvFSlu7k%3D

    CAS  Google Scholar 

  • W Seefelder M Gossmann H U Humpf (2002) ArticleTitleAnalysis of fumonisin B-1 in Fusarium proliferatum-infected asparagus spears and garlic bulbs from Germany by liquid chromatography – Electrospray ionization mass spectrometry J. Agric. Food Chem 50 2778–2781 Occurrence Handle1:CAS:528:DC%2BD38Xislahu7c%3D Occurrence Handle11982398

    CAS  PubMed  Google Scholar 

  • K A Seifert T Aoki R P Baayen D Brayford L W Burgess S Chulze W Gams D Geiser J Gruyter Particlede J F Leslie A Logrieco W F O Marasas H I Nirenberg K O’Donnell J Rheeder G J Samuels B A Summerell U Thrane C Waalwijk (2003) ArticleTitleThe nameFusarium moniliformae should no longer be used Mycol. Res 107 643–644

    Google Scholar 

  • R Singh B Rai (2000) ArticleTitleAntifungal potential of some higher plants against Fusarium udum causing wilt disease of Cajanus cajan Microbios 102 165–173 Occurrence Handle1:CAS:528:DC%2BD3cXltlSisL0%3D Occurrence Handle10955831

    CAS  PubMed  Google Scholar 

  • X C Souto F Pellissier (2002) Feedback mechanism in the chemical ecology of plants: role of soil microorganisms I Mallik A U Mallik (Eds) Chemical Ecology of Plants: Allelopathy in Aquatic and Terres trial Ecosystems Birkhauser Verlag Switzerland 89–97

    Google Scholar 

  • A Srobarova A Moretti R Ferracane A Ritieni A Logrieco (2002) ArticleTitleToxigenic Fusarium species of Liseola section in pre-harvest maize ear rot, and associated mycotoxins in Slovakia Eur. J. Plant Pathol 108 299–306 Occurrence Handle1:CAS:528:DC%2BD38XkvFersL0%3D

    CAS  Google Scholar 

  • M St-Arnaud C Hamel M Caron J A Fortin (1995) Endomycorrhizes V A et sensibilité aux maladies: Synthèse de la littérature et mécanismes d’interaction probables C Charest R Bernier (Eds) Mycorrhizal Symbiosis Orbis Frelighsburg,Québec 51–87

    Google Scholar 

  • M St-Arnaud C Hamel B Vimard M Caron J A Fortin (1996) ArticleTitleEnhanced hyphal and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots Mycol. Res 100 328–332

    Google Scholar 

  • M A Tabatabai (1982) Soil enzymes A L Page (Eds) Methods of Soil Analysis Part 2. Chemical and Microbiological Properties American Society of Agronomy Madison,WI,U.S.A. 903–947

    Google Scholar 

  • R P Voroney J P Winter R P Beyaert (1993) Soil microbial biomass C and N M Carter (Eds) Soil Sampling and Methods of Analysis CRC Press Boca Raton,U.S.A. 277–286

    Google Scholar 

  • V Vujanovic C Hamel S Jabaji-Hare M St-Arnaud (2002) ArticleTitleDevelopment of a selective myclobutanil agar (MBA) medium for the isolation of Fusarium species from asparagus fields Can. J. Microbiol 48 841–847 Occurrence Handle1:CAS:528:DC%2BD38XovVaqtrs%3D Occurrence Handle12455616

    CAS  PubMed  Google Scholar 

  • Vujanovic V, Hamel C, Yergeau E and St-Arnaud M 2004 Mycodiversity and mycogeography of Fusarium species from northeastern North American asparagus fields, based on microbiological and molecular approaches. Microbiol. Ecol. (in press).

  • T L Wacker G R Safir S N Stephenson (1990) ArticleTitleEvidence for succession of mycorrhizal fungi in Michigan asparagus fields Acta Agric. ISHS 271 273–278

    Google Scholar 

  • D R Walters (2003) ArticleTitlePolyamines and plant disease Phytochem 64 97–107 Occurrence Handle1:CAS:528:DC%2BD3sXms1Okur8%3D

    CAS  Google Scholar 

  • D D Warncke T C Reid M K Hausbeck (2002) ArticleTitleSodium chloride and lime effects on soil cations and elemental composition of asparagus fern Commun. Soil Sci. Plant Anal 33 3075–3084 Occurrence Handle1:CAS:528:DC%2BD38XptlKjt7c%3D

    CAS  Google Scholar 

  • D C White D B Ringelberg (1998) Signature lipid biomarker analysis R S Burlage R Atlas D Stahl G Geesey G Sayler (Eds) Techniques in Microbial Ecology Oxford University Press New York, U.S.A

    Google Scholar 

  • H Yao Z He M J wilson C D Campbell (2000) ArticleTitleMicrobial biomass and community structure in a sequence of soils with increasing fertility and changing land use Microb. Ecol 40 223–237 Occurrence Handle1:CAS:528:DC%2BD3cXptVWqt70%3D Occurrence Handle11080380

    CAS  PubMed  Google Scholar 

  • C C Young S H Chen (1987) ArticleTitlePhytotoxic study in the soil and root exudates of Asparagus officinalis L Asparagus Res. News 5 55–56

    Google Scholar 

  • C C Young T C Chou (1985) ArticleTitleAutointoxication in residues of Asparagus officinalis L Plant Soil 85 385–393

    Google Scholar 

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Authors and Affiliations

  1. Environmental Health / Water and Nutrients, Agriculture and Agri-Food Canada, 1 Airport Road Box 1030, Swift Current (SK), S9H 2X3, Canada

    C. Hamel

  2. Natural Resource Sciences, Macdonald Campus of McGill University, 21111 Lakeshore Road, Ste-Anne-de-Bellevue (QC), H9X 3V9, Canada

    C. Hamel, R. Jeannotte & A. Nakano-Hylander

  3. Institut de recherche en biologie végétale, Université de Montréal and Jardin botanique de Montréal, 4101 Sherbrooke est, Montréal (QC), H1X 2B2, Canada

    V. Vujanovic & M. St-Arnaud

  4. Microbial Ecology, Ecology Building, Lund University, SE-223 62, Lund, Sweden

    A. Nakano-Hylander

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  1. C. Hamel
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  2. V. Vujanovic
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  3. R. Jeannotte
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  4. A. Nakano-Hylander
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  5. M. St-Arnaud
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Correspondence to C. Hamel.

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Hamel, C., Vujanovic, V., Jeannotte, R. et al. 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, 75–87 (2005). https://doi.org/10.1007/s11104-004-0228-1

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