Skip to main content
SpringerLink
Log in

Groundcover management changes grapevine root fungal communities and plant-soil feedback

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

Abstract

Aims

The objective of this study was to determine if vineyard groundcover management can mitigate negative plant-soil feedback caused by soil borne pathogens through changes in root fungal communities.

Methods

Whole-soil inoculum was collected from a field trial of groundcover identity (exotic grasses, exotic grasses plus legumes, native grasses, and native grasses plus forbs) and irrigation type (drip, sprinkler, and a combination of both) in a modified feedback experiment with grapevine rootstock ‘101–14’ (Vitis riparia x V. rupestris). To see if these groundcovers would differ in their ability to protect vines against negative feedback caused by a soil borne pathogen, we inoculated all pots with the soil-borne root pathogen, Ilyonectria liriodendri (Halleen, Rego & Crous) Chaverri & C. Salgado.

Results

After eight months, vines growing with soil trained by exotic grasses had greater above-ground growth response relative to sterilized control than did vines growing with soil trained by native grasses and forbs. These treatments also resulted in compositionally distinct root fungal communities. The intensity of root colonization by arbuscular mycorrhizal fungi did not differ among ground cover treatments.

Conclusions

Our results show that soil feedback outcomes for grapevines, including negative effects of black foot pathogens such as Ilyonectria liriodendri, could depend on groundcover vegetation management that alters root-associated fungal communities.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agustí-Brisach C, Armengol J (2013) Black-foot disease of grapevine: an update on taxonomy, epidemiology and management strategies. Phytopathol Mediterr 52:245–261

    Google Scholar 

  • Agustí-Brisach C, Gramaje D, Leon M, Garcia-Jimenez J, Armengol J (2011) Evaluation of vineyard weeds as potential hosts of black-foot and petri disease pathogens. Plant Dis 95:803–810

    Article  Google Scholar 

  • Alaniz S, León M, Vicent A, García-Jiménez J, Abad-Campos P, Armengol J (2007) Characterization of species associated with black foot disease of grapevine in Spain. Plant Dis 91:1187–1193

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    Article  PubMed  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    Article  CAS  PubMed  Google Scholar 

  • Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321

    Article  CAS  Google Scholar 

  • Benitez MS, Taheri WI, Lehman RM (2016) Selection of fungi by candidate cover crops. Appl Soil Ecol 103:72–82

    Article  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  CAS  PubMed  Google Scholar 

  • Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977

    Article  Google Scholar 

  • Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J Ecol 94:893–904

    Article  CAS  Google Scholar 

  • Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744

    Article  CAS  PubMed  Google Scholar 

  • Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372

    Article  CAS  Google Scholar 

  • Casieri L, Hofstetter V, Viret O, Gindro K (2009) Fungal communities living in the wood of different cultivars of young Vitis vinifera plants. Phytopathol Mediterr 48:73–83

    Google Scholar 

  • De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    Article  PubMed  Google Scholar 

  • Druzhinina IS, Kopchinskiy AG, Komon M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828

    Article  CAS  PubMed  Google Scholar 

  • Eilers EJ, Klein AM (2009) Landscape context and management effects on an important insect pest and its natural enemies in almond. Biol Control 51:388–394

    Article  Google Scholar 

  • Fanin N, Haettenschwiler S, Fromin N (2014) Litter fingerprint on microbial biomass, activity, and community structure in the underlying soil. Plant Soil 379:79–91

    Article  CAS  Google Scholar 

  • Fourie P, Halleen F, van der Vyver J, Schreuder W (2001) Effect of Trichoderma treatments on the occurrence of decline pathogens in the roots and rootstocks of nursery grapevines. Phytopathol Mediterr 40:S473–S478

    Google Scholar 

  • Gonzalez V, Luisa Tello M (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42

    Article  Google Scholar 

  • Gramaje D, Armengol J (2011) Fungal trunk pathogens in the grapevine propagation process: potential inoculum sources, detection, identification, and management strategies. Plant Dis 95:1040–1055

    Article  Google Scholar 

  • Grayston SJ, Wang SQ, 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 

  • Halleen F, Crous PW, Petrini O (2003) Fungi associated with healthy grapevine cuttings in nurseries, with special reference to pathogens involved in the decline of young vines. Australas Plant Pathol 32:47–52

    Article  Google Scholar 

  • 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 268:75–87

    Article  CAS  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species - opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hartwig NL, Ammon HU (2002) Cover crops and living mulches. Weed Sci 50:688–699

    Article  CAS  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Hossain MM, Sultana F, Kubota M, Koyarna H, Hyakumachi M (2007) The plant growth-promoting fungus Penicillium simplicissimum GP17-2 induces resistance in Arabidopsis thaliana by activation of multiple defense signals. Plant Cell Physiol 48:1724–1736

    Article  CAS  PubMed  Google Scholar 

  • Inglis GD, Kawchuk LM (2002) Comparative degradation of oomycete, ascomycete, and basidiomycete cell walls by mycoparasitic and biocontrol fungi. Can J Microbiol 48:60–70

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586

    Article  Google Scholar 

  • Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G, Tzelepis GD, Nygren K, Dubey MK, Kamou N, Levasseur A, Zapparata A, Wang JH, Amby DB, Jensen B, Sarrocco S, Panteris E, Lagopodi AL, Poggeler S, Vannacci G, Collinge DB, Hoffmeister D, Henrissat B, Lee YH, Jensen DF (2015) Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol Evol 7:465–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Duenas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Luecking R, Martin MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Poldmaa K, Saag L, Saar I, Schuessler A, Scott JA, Senes C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Molec. Ecol 22:5271–5277

    CAS  Google Scholar 

  • Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek Int J Gen Molec Microbiol 73:331–371

    Article  CAS  Google Scholar 

  • Lange M, Habekost M, Eisenhauer N, Roscher C, Bessler H, Engels C, Oelmann Y, Scheu S, Wilcke W, Schulze E-D, Gleixner G (2014) Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS One 9:e96182. https://doi.org/10.1371/journal.pone.0096182

  • Latz E, Eisenhauer N, Rall BC, Allan E, Roscher C, Scheu S, Jousset A (2012) Plant diversity improves protection against soil-borne pathogens by fostering antagonistic bacterial communities. J Ecol 100:597–604

    Article  Google Scholar 

  • Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41

    Article  PubMed  Google Scholar 

  • McGonigle TP, Miller MH (2000) The inconsistent effect of soil disturbance on colonization of roots by arbuscular mycorrhizal fungi: a test of the inoculum density hypothesis. Appl Ecol 14:147–155

    Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Mueller A, Ngwene B, Peiter E, George E (2017) Quantity and distribution of arbuscular mycorrhizal fungal storage organs within dead roots. Mycorrhiza 27:201–210

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nicol RW, Yousef L, Traquair JA, Bernards MA (2003) Ginsenosides stimulate the growth of soilborne pathogens of American ginseng. Phytochemistry 64:257–264

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J et al (2016) Vegan: community ecology package. R package version 2:4–1 https://CRAN.R-project.org/package=vegan

    Google Scholar 

  • Palmborg C, Scherer-Lorenzen M, Jumpponen A, Carlsson G, Huss-Danell K, Hogberg P (2005) Inorganic soil nitrogen under grassland plant communities of different species composition and diversity. Oikos 110:271–282

    Article  CAS  Google Scholar 

  • Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas—functional processes and ecological impact. Springer, Berlin, pp 123–135

    Chapter  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rovira AD (1969) Plant root exudates. Bot Rev 35:35–53

  • Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122. https://doi.org/10.1186/s12862-016-0698-9

  • Schreiner RP, Koide RT (1993) Mustards, mustard oils, and mycorrhizas. New Phytol 123:107–113

  • Simon S, Bouvier JC, Debras JF, Sauphanor B (2010) Biodiversity and pest management in orchard systems. A review. Agron Sustain Dev 30:139–152

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New York

    Google Scholar 

  • Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998

    Article  Google Scholar 

  • Tabarant P, Villenave C, Risede JM, Roger-Estrade J, Dorel M (2011) Effects of organic amendments on plant-parasitic nematode populations, root damage, and banana plant growth. Biol Fertil Soil 47:341–347

    Article  Google Scholar 

  • Tukey JW (1949) Comparing individual means in the analysis of variance. Biometrics 5:99–114

    Article  CAS  PubMed  Google Scholar 

  • Úrbez-Torres JR, Haag P, Bowen P, O'Gorman DT (2014) Grapevine trunk diseases in British Columbia: incidence and characterization of the fungal pathogens associated with black foot disease of grapevine. Plant Dis 98:456–468

    Article  Google Scholar 

  • Úrbez-Torres JR, Haag P, Bowen P, Lowery T, O'Gorman DT (2015) Development of a DNA macroarray for the detection and identification of fungal pathogens causing decline of young grapevines. Phytopathology 105:1373–1388

    Article  PubMed  Google Scholar 

  • Vermeire M-L, Kablan L, Dorel M, Delvaux B, Risede J-M, Legreve A (2011) Protective role of silicon in the banana-Cylindrocladium spathiphylli pathosystem. Eur J Plant Pathol 131:621–630

    Article  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10

    Article  CAS  Google Scholar 

  • Vukicevich E, Lowery T, Bowen P, Urbez-Torres JR, Hart M (2016) Cover crops to increase soil microbial diversity and mitigate decline in perennial agriculture. A review Agron Sust Develop 36

  • Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135

    Article  PubMed  Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  Google Scholar 

  • White TJ, Burns T, Lee S, Taylor J (1990) Amplification and 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 315–322

  • Whitelaw-Weckert MA, Rahman L, Hutton RJ, Coombes N (2007a) Permanent swards increase soil microbial counts in two Australian vineyards. Appl Soil Ecol 36:224–232

    Article  Google Scholar 

  • Whitelaw-Weckert MA, Nair NG, Lamont R, Alonso M, Priest MJ, Huang R (2007b) Root infection of Vitis Vinifera by Cylindrocarpon liriodendri in Australia. Australas Plant Pathol 36:403–406

    Article  Google Scholar 

  • Whitelaw-Weckert MA, Rahman L, Appleby LM, Hall A, Clark AC, Waite H, Hardie WJ (2013) Co-infection by Botryosphaeriaceae and Ilyonectria Spp. Fungi during propagation causes decline of young grafted grapevines. Plant Pathol 62:1226–1237

    Article  Google Scholar 

  • Wright AJ, Wardle DA, Callaway R, Gaxiola A (2017) The overlooked role of facilitation in biodiversity experiments. Trend Ecol Evol 32:383–390

    Article  Google Scholar 

  • Yang H, Zang Y, Yuan Y, Tang J, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:50. https://doi.org/10.1186/1471-2148-12-50

Download references

Acknowledgements

This paper is dedicated to the memory of Diana Morales, who greatly enhanced both the content and enjoyment of this work. The authors also wish to acknowledge the funding sources that made this work possible. EV was supported by the British Columbia Wine Grape Council and the Growing Forward 2 program of Agriculture and Agri-Food Canada. MH was supported by the Organic Science Cluster/Growing Forward 2 program of Agriculture and Agri-Food Canada.

Author information

Authors and Affiliations

  1. Department of Biology, University of British Columbia – Okanagan, 3187 University Way, Kelowna, BC, V1V 1V7, Canada

    Eric Vukicevich & Miranda Hart

  2. Summerland Research and Development Centre, Agriculture and Agri-Food Canada, 4200 Highway 97 South, Summerland, BC, V0H 1Z0, Canada

    Eric Vukicevich, D. Thomas Lowery, José Ramón Úrbez-Torres & Pat Bowen

Authors
  1. Eric Vukicevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Thomas Lowery
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Ramón Úrbez-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pat Bowen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miranda Hart
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric Vukicevich.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Philippe Hinsinger

Electronic supplementary material

ESM 1

(DOCX 487 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vukicevich, E., Thomas Lowery, D., Úrbez-Torres, J.R. et al. Groundcover management changes grapevine root fungal communities and plant-soil feedback. Plant Soil 424, 419–433 (2018). https://doi.org/10.1007/s11104-017-3532-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3532-2

Keywords

Search

Navigation