Skip to main content

Advertisement

SpringerLink
Log in

Local diversity of native arbuscular mycorrhizal symbionts differentially affects growth and nutrition of three crop plant species

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

Abstract

Intact whole native AMF communities occurring across a 100-m-long field were used for the evaluation of plant performance, as determined by the actual fungal species colonizing host roots. The soil from distinct plots within a “hot spot” field was collected to set up 54 experimental units where three different plant species were grown, in order to test whether the whole native AMF communities were able to differentially affect plant growth, to assess the genetic identity of the AMF actually colonizing the tested plants and to analyse their community composition in the different hosts. Molecular analyses revealed that plant growth and nutrition of the crop plants were differentially affected by the diverse native arbuscular mycorrhizal communities colonizing the roots of the three plants, whose performance varied depending on the identity of plant hosts and fungal symbionts, more than on a rich and diversified AMF community. Such results, improving our understanding of AMF distribution at the local scale, represent a starting point allowing the selection, isolation and characterization of the most efficient AMF assemblages to be used as inoculants in sustainable food production systems.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abbott LK, Gazey C (1994) An ecological view of the formation of VA mycorrhizas. Plant Soil 159:69–78

    Article  Google Scholar 

  • Agnolucci M, Battini F, Cristani C, Giovannetti M (2015) Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fertil Soils 51:379–389

    Article  CAS  Google Scholar 

  • Alkan N, Gadkar V, Yarden O, Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microbiol 72:4192–4199

    Article  CAS  PubMed  PubMed Central  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 

  • Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR (2010) Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Curr Biol 20:1216–1221

    Article  CAS  PubMed  Google Scholar 

  • Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79

    Article  CAS  PubMed  Google Scholar 

  • Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci Rep 7:4686. https://doi.org/10.1038/s41598-017-04959-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Becklin KM, Hertweck KL, Jumpponen A (2012) Host identity impacts rhizosphere fungal communities associated with three alpine plant species. Microb Ecol 63:682–693

    Article  PubMed  Google Scholar 

  • Berruti A, Borriello R, Lumini E, Scariot V, Bianciotto V, Balestrini R (2013) Application of laser microdissection to identify the mycorrhizal fungi that establish arbuscules inside root cells. Front Plant Sci 4

  • Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21

    Article  PubMed  Google Scholar 

  • Błaszkowski J, Blanke V, Renker C, Buscot F (2004) Glomus aurantium and G. xanthium, new species in Glomeromycota. Mycotaxon 90:447–467

    Google Scholar 

  • Bremner JM, Mulvaney CS (1982) Nitrogen total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. American Society of Agronomy, Madison, WI, pp 595–624

    Google Scholar 

  • Brito I, Goss MJ, de Carvalho M, Chatagnier O, van Tuinen D (2012) Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil Till Res 121:63–67

    Article  Google Scholar 

  • Burrows RL, Pfleger FL (2002) Host responses to AMF from plots differing in plant diversity. Plant Soil 240:169–180

    Article  CAS  Google Scholar 

  • Carvalho LM, Correia PM, Ryel RJ, Martins-Loução MA (2003) Spatial variability of arbuscular mycorrhizal fungal spores in two natural plant communities. Plant Soil 251:227–236

    Article  CAS  Google Scholar 

  • Cesaro P, van Tuinen D, Copetta A, Chatagnier O, Berta G, Gianinazzi S, Lingua G (2008) Preferential colonization of Solanum tuberosum L roots by the fungus Glomus intraradices in arable soil of a potato farming area. Appl Environ Microbiol 74:5776–5783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeke TE, Schütte UM, Hemmerich CM, Cruzan MB, Rosenstiel TN, Bever JD (2015) Spatial soil heterogeneity has a greater effect on symbiotic arbuscular mycorrhizal fungal communities and plant growth than genetic modification with Bacillus thuringiensis toxin genes. Mol Ecol 24:2580–2593

    Article  CAS  PubMed  Google Scholar 

  • Croll D, Wille L, Gamper HA, Mathimaran N, Lammers PJ, Corradi N, Sanders IR (2008) Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 178:672–687

    Article  CAS  PubMed  Google Scholar 

  • Davison J, Moora M, Jairus T, Vasar M, Öpik M, Zobel M (2016) Hierarchical assembly rules in arbuscular mycorrhizal (AM) fungal communities. Soil Biol Biochem 97:63–70

    Article  CAS  Google Scholar 

  • Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier Ü, Saks Ü, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973

    Article  CAS  PubMed  Google Scholar 

  • Davison J, Öpik M, Daniell TM, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115

    Article  CAS  PubMed  Google Scholar 

  • De Beenhouwer M, Van Geel M, Ceulemans T, Muleta D, Lievens B, Honnay O (2015) Changing soil characteristics alter the arbuscular mycorrhizal fungi communities of Arabica coffee (Coffea arabica) in Ethiopia across a management intensity gradient. Soil Biol Biochem 91:133–139

    Article  Google Scholar 

  • Feddermann N, Boller T, Salzer P, Elfstrand S, Wiemken A, Elfstrand M (2008) Medicago truncatula shows distinct patterns of mycorrhiza-related gene expression after inoculation with three different arbuscular mycorrhizal fungi. Planta 227:671–680

    Article  CAS  PubMed  Google Scholar 

  • Gavito ME, Olsson PA (2008) Foraging strategies of the external mycelium of the arbuscular mycorrhizal fungi Glomus intraradices and Scutellospora calospora. Appl Soil Ecol 39:282–290

    Article  Google Scholar 

  • Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed) Methods of soil analysis, part 1. Physical and mineralogical methods. Agronomy monograph. 9, 2nd edn. American Society of Agronomy/Soil Science Society of America, Madison, WI, pp 383–411

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gustafson DJ, Casper BB (2006) Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: experimentally manipulating co-occurring Glomus species. Plant Ecol 183:257–263

    Article  Google Scholar 

  • Hart MM, Forsythe J, Oshowski B, Bücking H, Jansa J, Kiers ET (2013) Hiding in a crowd-does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis? Symbiosis 59:47–56

    Article  Google Scholar 

  • Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508

    Article  CAS  PubMed  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 

  • Hildebrandt U, Ouziad F, Marner F-JJ, Bothe H (2006) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett 254:258–267

    Article  CAS  PubMed  Google Scholar 

  • Hohnjec N, Vieweg ME, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansa J, Andrew SF, 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 

  • Jansa J, Erb A, Oberholzer H-R, Smilauer P, Egli S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:2118–2135

    Article  CAS  PubMed  Google Scholar 

  • Ji B, Bentivenga SP, Casper BB (2010) Evidence for ecological matching of whole AM fungal communities to the local plant-soil environment. Ecology 91:3037–3046

    Article  PubMed  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 

  • Jones J, Benton J, Wolf B, Mills HA (1991) Plant analysis handbook—a practical sampling, preparation, analysis, and interpretation guide. Micro-Macro Publishing Inc., Athens, USA

    Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303

    Article  CAS  Google Scholar 

  • Knegt B, Jansa J, Franken O, Engelmoer DJ, Werner GD, Bücking H, Kiers ET (2016) Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol 20:233–240

    Article  Google Scholar 

  • Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc Nat Acad Sci USA 101:2369–2374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Article  Google Scholar 

  • Koorem K, Tulva I, Davison J, Jairus T, Öpik M, Vasar M, Zobel M, Moora M (2017) Arbuscular mycorrhizal fungal communities in forest plant roots are simultaneously shaped by host characteristics and canopy-mediated light availability. Plant Soil 410:259–271

    Article  CAS  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748

    Article  CAS  PubMed  Google Scholar 

  • Massoumou M, van Tuinen D, Chatagnier O, Arnould C, Brechenmacher L, Sanchez L, Selim S, Gianinazzi S, Gianinazzi-Pearson V (2007) Medicago truncatula gene responses specific to arbuscular mycorrhiza interactions with different species and genera of Glomeromycota. Mycorrhiza 17:223–234

    Article  CAS  PubMed  Google Scholar 

  • Moora M, Öpik M, Sen R, Zobel M (2004) Native arbuscular mycorrhizal fungal communities differentially influence the seedling performance of rare and common Pulsatilla species. Funct Ecol 18:554–562

    Article  Google Scholar 

  • Morrison E, Lagos L, Al-Agely A, Glaab H, Johnson W, Jorquera MA, Ogram A (2017) Mycorrhizal inoculation increases genes associated with nitrification and improved nutrient retention in soil. Biol Fertil Soils 53:275–279

    Article  CAS  Google Scholar 

  • Mummey DL, Rillig MC (2008) Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiol Ecol 64:260–270

    Article  CAS  PubMed  Google Scholar 

  • Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853

    Article  CAS  PubMed  Google Scholar 

  • Nelson DW, Sommers L (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbiological properties, 2nd edn, Agronomy monograph 9 edn. American Society of Agronomy, Madison, WI, pp 539–579

  • Njeru EM, Avio L, Bocci G, Sbrana C, Turrini A, Bàrberi P, Giovannetti M, Oehl F (2015) Contrasting effects of cover crops on ‘hot spot’ arbuscular mycorrhizal fungal communities in organic tomato. Biol Fertil Soils 51:151–166

    Article  Google Scholar 

  • Njeru EM, Bocci G, Avio L, Sbrana C, Turrini A, Giovannetti M, Bàrberi P (2017) Functional identity has a stronger effect than diversity on mycorrhizal symbiosis and productivity of field grown organic tomato. Eur J Agron 86:1–11

    Article  Google Scholar 

  • Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738

    Article  CAS  Google Scholar 

  • Oehl F, Laczko E, Oberholzer HR, Jansa J, Egli S (2017) Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biol Fertil Soils. https://doi.org/10.1007/s00374-017-1217-x

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283

    Article  PubMed  Google Scholar 

  • Ohsowski BM, Zaitsoff PD, Öpik M, Hart MM (2014) Where the wild things are: looking for uncultured Glomeromycota. New Phytol 204:171–179

    Article  PubMed  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. Chemical and microbiological properties. Agronomy monograph 9, 2nd edn. American Society of Agronomy, Madison, WI, pp 403–430

    Google Scholar 

  • Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790

    Article  Google Scholar 

  • Pepe A, Sbrana C, Ferrol N, Giovannetti M (2017) An in vivo whole-plant experimental system for the analysis of gene expression in extraradical mycorrhizal mycelium. Mycorrhiza. https://doi.org/10.1007/s00572-017-0779-7

  • Pivato B, Mazurier S, Lemanceau P, Siblot S, Berta G, Mougel C, van Tuinen D (2007) Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol 176:197–210

    Article  CAS  PubMed  Google Scholar 

  • Pringle A, Bever JD (2002) Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am J Bot 89:1439–1446

    Article  PubMed  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Redecker D (2002) Molecular identification and phylogeny of arbuscular mycorrhizal fungi. Plant Soil 244:67–73

    Article  CAS  Google Scholar 

  • Redecker D, Hijri I, Wiemken A (2003) Molecular identification of arbuscular mycorrhizal fungi in roots: perspectives and problems. Folia Geobot 38:113–124

    Article  Google Scholar 

  • Rodríguez-Echeverría S, Teixeira H, Correia M, Timóteo S, Heleno R, Öpik M, Moora M (2017) Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytol 213:380–390

    Article  PubMed  Google Scholar 

  • Roger A, Colard A, Angelard C, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J 7:2137–2146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini F, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hort 196:91–108

    Article  Google Scholar 

  • Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546

    Article  CAS  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  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, .Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehlin J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    Article  PubMed  Google Scholar 

  • Stukenbrock EH, Rosendahl S (2005) Clonal diversity and population genetic structure of arbuscular mycorrhizal fungi (Glomus spp.) studied by multilocus genotyping of single spores. Mol Ecol 14:743–752

    Article  CAS  PubMed  Google Scholar 

  • Sumner ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. In: Sparks DL (ed) Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America, Madison, WI, pp 1201–1229

    Google Scholar 

  • Sýkorová Z, Wiemken A, Redecker A (2007) Co-occurring Gentiana verna and Gentiana acaulis and their neighboring plants in two Swiss Upper Montane meadows harbor distinct arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 73:5426–5434

    Article  PubMed  PubMed Central  Google Scholar 

  • Treseder KK, Cross A (2006) Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9:305–316

    Article  Google Scholar 

  • Turrini A, Agnolucci M, Palla M, Tomé E, Tagliavini M, Scandellari F, Giovannetti M (2017) Species diversity and community composition of native arbuscular mycorrhizal fungi in apple roots are affected by site and orchard management. Appl Soil Ecol 116:42–54

    Article  Google Scholar 

  • Turrini A, Avio L, Bedini S, Giovannetti M (2008) In situ collection of endangered arbuscular mycorrhizal fungi in a Mediterranean UNESCO Biosphere Reserve. Biodivers Conserv 17:643–657

    Article  Google Scholar 

  • Turrini A, Giovannetti M (2012) Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 22:81–97

    Article  PubMed  Google Scholar 

  • Turrini A, Sbrana C, Avio L, Njeru EM, Bocci G, Bàrberi P, Giovannetti M (2016) Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession. Biol Fertil Soils 52:643–653

    Article  Google Scholar 

  • Uibopuu A, Moora M, Öpik M, Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil 356:331–339

    Article  CAS  Google Scholar 

  • Vályi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytol 205:1577–1586

    Article  PubMed  Google Scholar 

  • Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Van der Gast CJ, Gosling P, Tiwari B, Bending GD (2011) Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice. Environ Microbiol 13:241–249

    Article  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 Geel M, Ceustermans A, Van Hemelrijck W, Lievens B, Honnay O (2015) Decrease in diversity and changes in community composition of arbuscular mycorrhizal fungi in roots of apple trees with increasing orchard management intensity across a regional scale. Mol Ecol 24:941–952

    Article  PubMed  Google Scholar 

  • Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562

    Article  PubMed  Google Scholar 

  • Walder F, van der Heijden MG (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants 1:15159

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Li X, Christie P, Zhang J, Li X (2016) Response of arbuscular mycorrhizal fungi to soil phosphorus patches depends on context. Crop Pasture Sci 67:1116–1125

    CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the University of Pisa through the project “Molecular and functional biodiversity of plant associated microrganisms” and through Fondi di Ateneo and by the National Research Council of Italy. The authors wish to thank Prof. Marco Mazzoncini and Dr. Rosalba Risaliti for their precious help in preserving the field site and determining soil physical and chemical properties.

Author information

Author notes

  1. Alessandra Turrini and Alberico Bedini contributed equally to this work.

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Alessandra Turrini, Alberico Bedini, Mario Bonilla Loor, Gaia Santini, Manuela Giovannetti & Luciano Avio

  2. INOQ GmbH, Schnega, and Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany

    Alberico Bedini

  3. Institute of Agricultural Biology and Biotechnology, CNR, UOS Pisa, Via Moruzzi 1, Pisa, Italy

    Cristiana Sbrana

Authors
  1. Alessandra Turrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberico Bedini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mario Bonilla Loor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gaia Santini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristiana Sbrana
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Manuela Giovannetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luciano Avio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Alessandra Turrini or Luciano Avio.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 114 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turrini, A., Bedini, A., Loor, M.B. et al. Local diversity of native arbuscular mycorrhizal symbionts differentially affects growth and nutrition of three crop plant species. Biol Fertil Soils 54, 203–217 (2018). https://doi.org/10.1007/s00374-017-1254-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-017-1254-5

Keywords

Search

Navigation