Plant and Soil

, Volume 424, Issue 1–2, pp 419–433 | Cite as

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

  • Eric Vukicevich
  • D. Thomas Lowery
  • José Ramón Úrbez-Torres
  • Pat Bowen
  • Miranda Hart
Regular Article



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.


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.


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.


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.


Black-foot disease Cover crops Fungal ecology Plant-soil feedback Vineyards 



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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11104_2017_3532_MOESM1_ESM.docx (488 kb)
ESM 1 (DOCX 487 kb)


  1. Agustí-Brisach C, Armengol J (2013) Black-foot disease of grapevine: an update on taxonomy, epidemiology and management strategies. Phytopathol Mediterr 52:245–261Google Scholar
  2. 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 95:803–810CrossRefGoogle Scholar
  3. 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 91:1187–1193Google Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215:403–410CrossRefPubMedGoogle Scholar
  5. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525CrossRefGoogle Scholar
  6. 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 141:221–235CrossRefPubMedGoogle Scholar
  7. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681CrossRefPubMedGoogle Scholar
  8. Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321CrossRefGoogle Scholar
  9. Benitez MS, Taheri WI, Lehman RM (2016) Selection of fungi by candidate cover crops. Appl Soil Ecol 103:72–82CrossRefGoogle Scholar
  10. 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 68:1–13CrossRefPubMedGoogle Scholar
  11. Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977CrossRefGoogle Scholar
  12. 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 94:893–904CrossRefGoogle Scholar
  13. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744CrossRefPubMedGoogle Scholar
  14. Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545CrossRefPubMedPubMedCentralGoogle Scholar
  15. Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372CrossRefGoogle Scholar
  16. 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 48:73–83Google Scholar
  17. De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574CrossRefPubMedGoogle Scholar
  18. 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 42:813–828CrossRefPubMedGoogle Scholar
  19. Eilers EJ, Klein AM (2009) Landscape context and management effects on an important insect pest and its natural enemies in almond. Biol Control 51:388–394CrossRefGoogle Scholar
  20. Fanin N, Haettenschwiler S, Fromin N (2014) Litter fingerprint on microbial biomass, activity, and community structure in the underlying soil. Plant Soil 379:79–91CrossRefGoogle Scholar
  21. 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–S478Google Scholar
  22. Gonzalez V, Luisa Tello M (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42CrossRefGoogle Scholar
  23. Gramaje D, Armengol J (2011) Fungal trunk pathogens in the grapevine propagation process: potential inoculum sources, detection, identification, and management strategies. Plant Dis 95:1040–1055CrossRefGoogle Scholar
  24. Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  25. 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 32:47–52CrossRefGoogle Scholar
  26. 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
  27. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species - opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56CrossRefPubMedGoogle Scholar
  28. Hartwig NL, Ammon HU (2002) Cover crops and living mulches. Weed Sci 50:688–699CrossRefGoogle Scholar
  29. 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 13:394–407CrossRefPubMedGoogle Scholar
  30. 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 48:1724–1736CrossRefPubMedGoogle Scholar
  31. Inglis GD, Kawchuk LM (2002) Comparative degradation of oomycete, ascomycete, and basidiomycete cell walls by mycoparasitic and biocontrol fungi. Can J Microbiol 48:60–70CrossRefPubMedGoogle Scholar
  32. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  33. 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 7:465–480CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 22:5271–5277Google Scholar
  35. 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 73:331–371CrossRefGoogle Scholar
  36. 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.
  37. 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 100:597–604CrossRefGoogle Scholar
  38. Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41CrossRefPubMedGoogle Scholar
  39. 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 14:147–155Google Scholar
  40. 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 115:495–501CrossRefGoogle Scholar
  41. Mueller A, Ngwene B, Peiter E, George E (2017) Quantity and distribution of arbuscular mycorrhizal fungal storage organs within dead roots. Mycorrhiza 27:201–210CrossRefGoogle Scholar
  42. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  43. Nicol RW, Yousef L, Traquair JA, Bernards MA (2003) Ginsenosides stimulate the growth of soilborne pathogens of American ginseng. Phytochemistry 64:257–264CrossRefPubMedGoogle Scholar
  44. Oksanen J et al (2016) Vegan: community ecology package. R package version 2:4–1 Google Scholar
  45. 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 110:271–282CrossRefGoogle Scholar
  46. 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 123–135CrossRefGoogle Scholar
  47. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. Rovira AD (1969) Plant root exudates. Bot Rev 35:35–53Google Scholar
  49. 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.
  50. Schreiner RP, Koide RT (1993) Mustards, mustard oils, and mycorrhizas. New Phytol 123:107–113Google Scholar
  51. Simon S, Bouvier JC, Debras JF, Sauphanor B (2010) Biodiversity and pest management in orchard systems. A review. Agron Sustain Dev 30:139–152CrossRefGoogle Scholar
  52. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New YorkGoogle Scholar
  53. Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998CrossRefGoogle Scholar
  54. 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 47:341–347CrossRefGoogle Scholar
  55. Tukey JW (1949) Comparing individual means in the analysis of variance. Biometrics 5:99–114CrossRefPubMedGoogle Scholar
  56. 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 98:456–468CrossRefGoogle Scholar
  57. 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 105:1373–1388CrossRefPubMedGoogle Scholar
  58. 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 131:621–630CrossRefGoogle Scholar
  59. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedPubMedCentralGoogle Scholar
  60. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10CrossRefGoogle Scholar
  61. 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 36Google Scholar
  62. Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135CrossRefPubMedGoogle Scholar
  63. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227CrossRefGoogle Scholar
  64. 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 315–322Google Scholar
  65. Whitelaw-Weckert MA, Rahman L, Hutton RJ, Coombes N (2007a) Permanent swards increase soil microbial counts in two Australian vineyards. Appl Soil Ecol 36:224–232CrossRefGoogle Scholar
  66. 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 36:403–406CrossRefGoogle Scholar
  67. 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 62:1226–1237CrossRefGoogle Scholar
  68. Wright AJ, Wardle DA, Callaway R, Gaxiola A (2017) The overlooked role of facilitation in biodiversity experiments. Trend Ecol Evol 32:383–390CrossRefGoogle Scholar
  69. 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.

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Eric Vukicevich
    • 1
    • 2
  • D. Thomas Lowery
    • 2
  • José Ramón Úrbez-Torres
    • 2
  • Pat Bowen
    • 2
  • Miranda Hart
    • 1
  1. 1.Department of BiologyUniversity of British Columbia – OkanaganKelownaCanada
  2. 2.Summerland Research and Development Centre, Agriculture and Agri-Food CanadaSummerlandCanada

Personalised recommendations