Skip to main content
Log in

How distinct are arbuscular mycorrhizal fungal communities associating with grapevines?

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

Abstract

Grapevines form associations with arbuscular mycorrhizal (AM) fungi. These root-dwelling fungi have the potential to contribute to crop vigor, productivity, pathogen protection, and nutrient content in grapes. In this study the arbuscular mycorrhizal fungal communities of grapevines and the surrounding interrow and native vegetation are compared. We found over 40 different taxa associating with both vines and interrow vegetation, but these communities differed based on host plant identity. These differences were apparent even after accounting for differences in soil chemical properties and differences in host plant diversity between vinerows and interrows, indicating that Vitis preferentially interacts with a subset of the viticultural fungal community. Since AM fungal communities play a major role in grapevine health, our results suggest that host identity and the diversity of AM fungal hosts in a vineyard can have strong effects on arbuscular mycorrhizal fungi community structure. In this paper, we used high throughput sequencing of the large subunit rDNA to analyze the diversity of AM fungi growing in a vineyard.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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
Fig. 6

Similar content being viewed by others

References

  • Alguacil MM, Torres MP, Torrecillas E, Diaz G, Roland A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173

    Article  CAS  Google Scholar 

  • Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47–62

    Article  CAS  Google Scholar 

  • An GH, Miyakawa S, Kawahara A, Osaki M, Ezawa T (2008) Community structure of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci Plant Nut 54:517–528

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Balestrini R, Magurno F, Walker C, Lumini E, Bianciotto V (2010) Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop. Environ Microbiol Reports 2:594–604

    Article  Google Scholar 

  • Baslam M, Goicoechea N (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22:347–359

    Article  CAS  PubMed  Google Scholar 

  • Bowen, P, C Bogdanoff, K Usher, T Lowery, M Cliff, Neilsen G (2012) Irrigation regimes affect soil wetting patterns, leaf gas exchange, berry composition, and wine quality in Merlot, Syrah and Cabernet Sauvignon Report to AAFC and BCWGC for MII project A07344 (published on line at www.bbcgc.org). Accessed 18 Apr 2013

  • 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 Central  PubMed  Google Scholar 

  • Cangahuala-Inocente GC, Da Silva MF, Johnson J, Manga A, van Tuinen D, Henry C, Lovato PE, Dumas-Gaudot E (2011) Arbuscular mycorrhizal symbiosis elicits proteome responses opposite of P-starvation in SO4 grapevine rootstock upon root colonization with two Glomus species. Mycorrhiza 21:473–493

    Article  CAS  PubMed  Google Scholar 

  • Caporaso GJ, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods. doi:101038/nmethf303

    PubMed Central  PubMed  Google Scholar 

  • Cesco SM, Nunni TG, Tomasi R, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bioactivities related to plant nutrition. Biol Fert Soils 48:123–150

    Article  CAS  Google Scholar 

  • Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chan 13:980–989

    Article  Google Scholar 

  • Daubenmire R (1957) A canopy coverage method of vegetational analysis. Northwest Science 33:43–64

    Google Scholar 

  • De Deyn GB, Quirk H, Bardgett RD (2011) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 7:75–78

    Article  PubMed Central  PubMed  Google Scholar 

  • Dhillion SS (1992) Evidence for host mycorrhizal preference in native grassland species. Mycol Res 96:359–362

    Article  Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. The ISME J 4:337–345

    Article  Google Scholar 

  • Douds DD, Millner PD (1999) Biodiversity of arbuscular mycorrhizal fungi in agro ecosystems. Agric Ecosyst and Environ 74:77–93

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Fitzsimons MS, Miller RM, Jastrow JD (2008) Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158:117–127

    Article  PubMed  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Winf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonizing roots of the grass species Agrostis capillaries and Lolium perenne in a field experiment. Mycorrhiza 14:111–117

    Article  PubMed  Google Scholar 

  • Hart MM, Trevors JT (2005) The practical application of mycorrhizas, what are we waiting for? Front Ecol Environ 3:533–539

    Article  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2008) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  Google Scholar 

  • Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384

    Article  Google Scholar 

  • Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362

    Article  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi. New Phytol 177:779–789

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Tillman D, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042

    Article  Google Scholar 

  • Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515

    Article  Google Scholar 

  • Klironomos JN, Hart MM, Gurney JE, Moutoglis P (2001) Interspecific differences in the tolerance of arbuscular mycorrhizal fungi to freezing and drying. Can J Bot 79:1161–1166

    Article  Google Scholar 

  • Krüger M, Krüger C, Walker SH, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984

    Article  PubMed  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Boston

    Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433. doi:101038/ismej201341

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, Zheng CC (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47:154–163

    Article  CAS  PubMed  Google Scholar 

  • Linderman RG, Davis AE (2001) Comparative response of selected grapevine rootstocks and cultivars to inoculation with different mycorrhizal fungi. Am J Enol Viticult 52:8–11

    CAS  Google Scholar 

  • Lozupone CA, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pytosequencing approach. Environ Microbiol 12:2165–2179

    CAS  PubMed  Google Scholar 

  • Menge JA, Raski DJ, Lider LA, Johnson ELV, Jones NO, Kissler JJ, Hemstreet CL (1983) Interactions between mycorrhizal fungi, soil fumigation and growth of grapes in California. Am J Enol Viticult 34:117–121

    Google Scholar 

  • Mohr HD (1996) Periodicity of root tip growth of vines in the Moselle valley. Vitic and Enol Sci 51:83–90

    Google Scholar 

  • Newsham K, Fitter A, Watkinson A (1995) Multifunctionality and biodiversity in arbuscular mycorrhizas. Trends Ecol and Evol 10:407–411

    Article  CAS  Google Scholar 

  • Nogales A, Aguirreolea J, Maria ES, Camprubi A, Calvet C (2009a) Response of mycorrhizal grapevine to Armillaria mellea inoculation: disease development and polyamines. Plant Soil 317:177–187

    Article  CAS  Google Scholar 

  • Nogales A, Luque J, Estaún V, Camprubi A, Garcia-Figueres F, Calvet C (2009b) Differential growth of mycorrhizal field-inoculated grapevine rootstocks in two replant soils. Am J Enol Vitic 60:484–489

    CAS  Google Scholar 

  • R Development Core Team (2008) R version 281 R Foundation for Statistical Computing, Vienna, Austria wwwr-projectorgi. Accessed 16 Feb 2013

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178(2):253–266

    Article  PubMed  Google Scholar 

  • Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schreiner PR (2005a) Mycorrhizas and mineral acquisition. In: Christensen LP, Smart DR (eds) Grapevines proceedings of the soil environment and vine mineral nutrition symposium. American Society of Enology and Viticulture, Davis, pp 49–60

    Google Scholar 

  • Schreiner RP (2005b) Spatial and temporal variation of roots, arbuscular mycorrhizal fungi, and plant and soil nutrients in a mature Pinot noir (Vitis vinifera L) vineyard in Oregon, USA. Plant Soil 276:219–234

    Article  CAS  Google Scholar 

  • Schreiner PR (2007) Effects of native and nonnative arbuscular mycorrhizal fungi on growth and nutrient uptake of ‘Pinot noir’ (Vitis vinifera L) in two soils with contrasting levels of phosphorus. Appl Soil Ecology 36:205–215

    Article  Google Scholar 

  • Schreiner RP, Linderman RG (2005) Mycorrhizal colonization in dryland vineyards of the Willamette Valley, Oregon. Small Fruits Review 4:41–55

    Article  Google Scholar 

  • Schreiner PR, Mihara KL (2009) The diversity of arbuscular mycorrhizal fungi amplified from grapevine roots (Vitis vinifera L) in Oregon vineyards is seasonally stable and influenced by soil and vine age. Mycologia 101:599–611

    Article  PubMed  Google Scholar 

  • Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytol 131:247–254

    Article  Google Scholar 

  • Seguin G (1986) ‘Terroirs’ and pedology of wine growing. Experientia 42:861–873

    Article  CAS  Google Scholar 

  • Sikes BA (2010) When do arbuscular mycorrhizal fungi protect plant roots from pathogens? Plant Sign Behav 5:763–765

    Article  Google Scholar 

  • Smart RE, Coombe BG (1983) Water relations of grapevines. In: Kozlowski TT (ed) Water deficits and plant growth. Academic, New York, pp 137–196

    Google Scholar 

  • Smith SE, Smith AF, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphorous supply to plants irrespective of growth response. Plant Physiol 133(1):16–20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13

    Article  PubMed  Google Scholar 

  • Torrecillas E, Alguacil M, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous pant species in semiarid Mediterranean prairies. Appl Environ Microbiol. doi:101128/AEM01287-12

    PubMed Central  PubMed  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Strallen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • van Leeuwen C, Friant P, Chone X, Tregoat O, Koundouras S, Dubourdieu D (2004) Influence of climate, soil and cultivar on terroir. Am J Enol Vitic 55:207–217

    Google Scholar 

  • Valentine AJ, Mortimer PE, Lintnaar M, Borgo R (2006) Drought responses of arbuscular mycorrhizal grapevines. Symbiosis 41(3):127–133

    CAS  Google Scholar 

  • Veiga RSL, Jansa J, Frossard E, van der Heijden MGA (2011) Can Arbuscular Mycorrhizal Fungi Reduce the Growth of Agricultural Weeds? PLoS ONE 6:e27825. doi:101371/journalpone0027825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with non-native plants and contribute to plant invasion. Ecology 90:399–407

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the NSERC CGS scholarship (TH), the NSERC Discovery Grant Program (MH), the BC Wine Grape Council, Agriculture and Agri-Food Canada's Matching Investment Initiative (PB and CB) and SunRock Vineyard.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miranda M. Hart.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESMTable 1

(DOCX 67 kb)

ESMTable 2

(DOCX 29 kb)

ESMTable 3

(DOCX 52 kb)

ESMTable 4

(DOCX 61 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holland, T.C., Bowen, P., Bogdanoff, C. et al. How distinct are arbuscular mycorrhizal fungal communities associating with grapevines?. Biol Fertil Soils 50, 667–674 (2014). https://doi.org/10.1007/s00374-013-0887-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-013-0887-2

Keywords

Navigation