Advertisement

Biology and Fertility of Soils

, Volume 52, Issue 5, pp 643–653 | Cite as

Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession

  • Alessandra TurriniEmail author
  • Cristiana Sbrana
  • Luciano Avio
  • Ezekiel Mugendi Njeru
  • Gionata Bocci
  • Paolo Bàrberi
  • Manuela Giovannetti
Original Paper

Abstract

Arbuscular mycorrhizal fungi (AMF) establish mutualistic associations with the most important agricultural food and feed crops, sustaining plant growth, nutrient uptake and tolerance of biotic and abiotic stresses. Scanty information is available on the role played by crop identity and diversity as a driving force shaping AMF species communities in the field, in particular in low-input and organic farming, where crop rotation and the use of cover crops are common practices. Here, using a molecular approach, we investigated whether plant communities established in low and high diversity cover crop treatments affect the composition of native AMF root communities of subsequent maize in a Mediterranean organic agroecosystem. A total of 16 AMF sequence types were detected, with Acaulospora cavernata as the most abundant phylotype, accounting for 37.4 % of the sequences, followed by Funneliformis mosseae, Claroideoglomus lamellosum and Rhizoglomus intraradices. Sequences matching to Funneliformis caledonium, Diversispora aurantia, Diversispora epigaea and Archaeospora schenckii corresponded to less than 2.0 % of the total. The most abundant sequences retrieved in plants from cover crop treatments were represented by A. cavernata, while sequences in maize roots were related to F. mosseae, R. intraradices and Glomus sp. Such data show for the first time a change in the composition of native AMF communities colonizing maize roots, which was independent of the identity and diversity of the preceding crop. Our findings suggest that host preference may represent a strong driver of AMF community dynamics in agroecosystems, differentially boosting or depressing AMF species, possibly in relation to their functional significance.

Keywords

Arbuscular mycorrhizal fungi Cover crop diversity AMF diversity Glomeromycota Small ribosomal subunit (SSU rDNA) Native AMF communities 

Notes

Acknowledgments

This work was funded by the EU-RTD FP7 Project SOLIBAM (Strategies for Organic and Low-input Integrated Breeding and Management), GrantAgreement FP7-KBBE 245058, 2010–2014, by the University of Pisa and National Research Council. The PhD grant of E.M. Njeru was funded by the International PhD Programme in Agrobiodiversity of the Scuola Superiore Sant’Anna of Pisa, Italy. The authors wish to thank Giacomo Nardi and the CIRAA personnel for their precious help in carrying out the field experiment.

Authorship and contributorship

A.T., C.S., L.A. and M.G. conceived and designed the experiments. A.T. and C.S. performed molecular and data analyses. L.A. performed data analyses. A.T., L.A. and M.G. wrote the paper. P.B., G.B. and E.M.N. provided the experimental system and agronomic expertise, and revised the paper. M.G. contributed reagents/materials/analysis tools.

Supplementary material

374_2016_1106_MOESM1_ESM.pptx (130 kb)
ESM 1 (PPTX 130 kb)

References

  1. 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 51:379–389CrossRefGoogle Scholar
  2. Akiyama K, Ken-ichi M, Hideo H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827CrossRefPubMedGoogle Scholar
  3. Alguacil MM, Torrecillas E, García-Orenes F, Roldán A (2014) Changes in the composition and diversity of AMF communities mediated by management practices in a Mediterranean soil are related with increases in soil biological activity. Soil Biol Biochem 76:34–44CrossRefGoogle Scholar
  4. 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 20:1216–1221CrossRefPubMedGoogle Scholar
  5. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172:347–357CrossRefPubMedGoogle Scholar
  6. 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 Rep 2:594–604CrossRefPubMedGoogle Scholar
  7. Becklin KM, Hertweck KL, Jumpponen A (2012) Host identity impacts rhizosphere fungal communities associated with three alpine plant species. Microb Ecol 63:682–693CrossRefPubMedGoogle Scholar
  8. Blanke V, Wagner M, Renker C, Lippert H, Michulitz M, Kuhn A, Buscot F (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392CrossRefGoogle Scholar
  9. Błaszkowski J (1993) Comparative studies of the occurrence of arbuscular fungi and mycorrhizae (Glomales) in cultivated and uncultivated soils of Poland. Acta Mycol 28:93–140CrossRefGoogle Scholar
  10. Błaszkowski J, Blanke V, Renker C, Buscot F (2004) Glomus aurantium and G xanthium, new species in Glomeromycota. Mycotaxon 90:447–467Google Scholar
  11. 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 Tillage Res 121:63–67CrossRefGoogle Scholar
  12. Castillo CG, Rubio R, Rouanet JL, Borie F (2006) Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an ultisol. Biol Fertil Soils 43:83–92CrossRefGoogle Scholar
  13. 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 74:5776–5783CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67CrossRefGoogle Scholar
  15. Davison J, Opik M, Daniell TM, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115CrossRefPubMedGoogle Scholar
  16. Douds DD Jr, Galvez L, Janke RR, Wagoner P (1995) Effect of tillage and farming system upon populations and distribution of vesicular-arbuscular mycorrhizal fungi. Agric Ecosyst Environ 52:111–118CrossRefGoogle Scholar
  17. Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804CrossRefPubMedGoogle Scholar
  18. 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 227:671–680CrossRefPubMedGoogle Scholar
  19. 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 20:519–530CrossRefPubMedGoogle Scholar
  20. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593CrossRefGoogle Scholar
  21. Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP (2001) The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717–724CrossRefGoogle Scholar
  22. 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 14:111–117CrossRefPubMedGoogle Scholar
  23. Gosling P, Mead A, Proctor M, Hammond JP, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hausmann NT, Hawkes CV (2009) Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol 183:1188–1200CrossRefPubMedGoogle Scholar
  25. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431CrossRefPubMedGoogle Scholar
  26. Helgason T, Fitter AH, Young JPW (1999) Molecular diversity of arbuscular mycorrhizal fungi colonising Hyacinthoides non-scripta (bluebell) in a seminatural woodland. Mol Ecol 8:659–666CrossRefGoogle Scholar
  27. 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 90:371–384CrossRefGoogle Scholar
  28. Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938CrossRefPubMedGoogle Scholar
  29. Higo M, Isobe K, Drijber RA, Kondo T, Yamaguchi M, Takeyama S, Suzuki Y, Niijima D, Matsuda Y, Ishii R, Torigoe Y (2014) Impact of a 5-year winter cover crop rotational system on the molecular diversity of arbuscular mycorrhizal fungi colonizing roots of subsequent soybean. Biol Fertil Soils 50:913–926CrossRefGoogle Scholar
  30. Higo M, Isobe K, Kondo T, Yamaguchi M, Takeyama S, Drijber RA, Torigoe Y (2015) Temporal variation of the molecular diversity of arbuscular mycorrhizal communities in three different winter cover crop rotational systems. Biol Fertil Soils 51:21–32CrossRefGoogle Scholar
  31. Hijri I, Sykorova Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289CrossRefPubMedGoogle Scholar
  32. 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 254:258–267CrossRefPubMedGoogle Scholar
  33. 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 137:1283–1301CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structures of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176CrossRefGoogle Scholar
  35. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757CrossRefGoogle Scholar
  36. Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908CrossRefGoogle Scholar
  37. Kabir Z, Koide RT (2002) Effect of autumn and winter mycorrhizal cover crops on soil properties, nutrient uptake and yield of sweet corn in Pennsylvania, USA. Plant Soil 238:205–215CrossRefGoogle Scholar
  38. Lehman RM, Taheri WI, Osborne SL, Buyer JS, Douds DD Jr (2012) Fall cover cropping can increase arbuscular mycorrhizae in soils supporting intensive agricultural production. Appl Soil Ecol 61:300–304CrossRefGoogle Scholar
  39. 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 17:223–234CrossRefPubMedGoogle Scholar
  40. Mathimaran N, Ruh R, Jama B, Verchot L, Frossard E, Jansa J (2007) Impact of agricultural management on arbuscular mycorrhizal fungal communities in Kenyan ferralsol. Agric Ecosyst Environ 119:22–32CrossRefGoogle Scholar
  41. Mello A, Lumini E, Napoli C, Bianciotto V, Bonfante P (2015) Arbuscular mycorrhizal fungal diversity in the Tuber melanosporum brûlé. Fungal Biol 119:518–527CrossRefPubMedGoogle Scholar
  42. Montero Sommerfeld H, Díaz LM, Alvarez M, Añazco Villanueva C, Matus F, Boon N, Boeckx P, Huygens D (2013) High winter diversity of arbuscular mycorrhizal fungal communities in shallow and deep grassland soils. Soil Biol Biochem 65:236–244CrossRefGoogle Scholar
  43. Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, Verdú M (2012) Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi. New Phytol 196:835–844CrossRefPubMedGoogle Scholar
  44. Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90CrossRefGoogle Scholar
  45. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  46. Na Bhadalung N, Suwanarit A, Dell B, Nopamornbodi O, Thamchaipenet A, Rungchuang J (2005) Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize cropping system. Plant Soil 270:371–382CrossRefGoogle Scholar
  47. Njeru EM, Avio L, Sbrana C, Turrini A, Bocci G, Bàrberi P, Giovannetti M (2014) First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron Sustain Dev 34:841–848CrossRefGoogle Scholar
  48. 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 51:151–166CrossRefGoogle Scholar
  49. 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 69:2816–2824CrossRefPubMedPubMedCentralGoogle Scholar
  50. Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583CrossRefPubMedGoogle Scholar
  51. 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 165:273–283CrossRefPubMedGoogle Scholar
  52. Pimentel D, Wilson C, McCullum C, Huang R, Dwen P, Flack J, Tran Q, Saltman T, Cliff B (1997) Economic and environmental benefits of biodiversity. Bioscience 47:747–757CrossRefGoogle Scholar
  53. Redecker D, Schüßler A, Stockinger H, Stürmer SR, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531CrossRefPubMedGoogle Scholar
  54. Reinhart KO, Brian LA (2014) More closely related plants have more distinct mycorrhizal communities. AoB Plants 6:plu051CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546CrossRefPubMedGoogle Scholar
  56. Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794Google Scholar
  57. 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 70:6240–6246CrossRefPubMedPubMedCentralGoogle Scholar
  58. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  59. 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 73:5426–5434CrossRefPubMedPubMedCentralGoogle Scholar
  60. Toljander JF, Santos-Gonzalez JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338CrossRefPubMedGoogle Scholar
  61. Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78:6180–6186CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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 205:1577–1586CrossRefPubMedGoogle Scholar
  63. 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 396:69–72CrossRefGoogle Scholar
  64. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095CrossRefPubMedGoogle Scholar
  65. Veresoglou SD, Rillig MC (2014) Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis. Plant Soil 377:395–406CrossRefGoogle Scholar
  66. Weil R, Kremen A (2007) Thinking across and beyond disciplines to make cover crops pay. J Sci Food Agric 87:551–557CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alessandra Turrini
    • 1
    Email author
  • Cristiana Sbrana
    • 2
  • Luciano Avio
    • 2
  • Ezekiel Mugendi Njeru
    • 3
  • Gionata Bocci
    • 4
  • Paolo Bàrberi
    • 4
  • Manuela Giovannetti
    • 1
  1. 1.Dipartimento di Scienze Agrarie, Alimentari e Agro-ambientaliUniversità di PisaPisaItaly
  2. 2.Istituto di Biologia e Biotecnologia Agraria, CNR, UO PisaPisaItaly
  3. 3.Department of MicrobiologyKenyatta UniversityNairobiKenya
  4. 4.Istituto di Scienze della Vita, Scuola Superiore Sant’AnnaPisaItaly

Personalised recommendations