Journal of Microbiology

, Volume 54, Issue 2, pp 86–97 | Cite as

Molecular diversity and distribution of indigenous arbuscular mycorrhizal communities colonizing roots of two different winter cover crops in response to their root proliferation

  • Masao Higo
  • Katsunori Isobe
  • Yusuke Miyazawa
  • Yukiya Matsuda
  • Rhae A. Drijber
  • Yoichi Torigoe
Microbial Ecology and Environmental Microbiology
First Online:
Received:
Revised:
Accepted:

Abstract

A clear understanding of how crop root proliferation affects the distribution of the spore abundance of arbuscular mycorrhizal fungi (AMF) and the composition of AMF communities in agricultural fields is imperative to identify the potential roles of AMF in winter cover crop rotational systems. Toward this goal, we conducted a field trial using wheat (Triticum aestivum L.) or red clover (Trifolium pratense L.) grown during the winter season. We conducted a molecular analysis to compare the diversity and distribution of AMF communities in roots and spore abundance in soil cropped with wheat and red clover. The AMF spore abundance, AMF root colonization, and abundance of root length were investigated at three different distances from winter crops (0 cm, 7.5 cm, and 15 cm), and differences in these variables were found between the two crops. The distribution of specific AMF communities and variables responded to the two winter cover crops. The majority of Glomerales phylotypes were common to the roots of both winter cover crops, but Gigaspora phylotypes in Gigasporales were found only in red clover roots. These results also demonstrated that the diversity of the AMF colonizing the roots did not significantly change with the three distances from the crop within each rotation but was strongly influenced by the host crop identity. The distribution of specific AMF phylotypes responded to the presence of wheat and red clover roots, indicating that the host crop identity was much more important than the proliferation of crop roots in determining the diversity of the AMF communities.

Keywords

arbuscular mycorrhizal fungi community structure cover crops host identity root distribution 
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References

  1. Avio, L., Castaldini, M., Fabiani, A., Bedini, S., Sbrana, C., Turrini, A., and Giovannetti, M. 2013. Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol. Biochem. 67, 285–294.CrossRefGoogle Scholar
  2. Azcón-Aguilar, C. and Barea, J.M. 1981. Field inoculation of Medicago with V-A mycorrhiza and Rhizobium in phosphate-fixing agricultural soil. Soil Biol. Biochem. 13, 19–22.CrossRefGoogle Scholar
  3. Bainard, L.D., Bainard, J.D., Hamel, C., and Gan, Y. 2014. Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semi-arid prairie agroecosystem. FEMS Microbiol. Ecol. 88, 333–344.CrossRefPubMedGoogle Scholar
  4. Bainard, L.D., Dai, M., Gomez, E.F., Torres-Arias, Y., Bainard, J.D., Sheng, M., Eilers, W., and Hamel, C. 2015. Arbuscular mycorrhizal fungal communities are influenced by agricultural land use and not soil type among the Chernozem great groups of the Canadian Prairies. Plant Soil 387, 351–362.CrossRefGoogle Scholar
  5. Bainard, L.D., Koch, A.M., Gordon, A.M., Newmaster, S.G., Thevathasan, N.V., and Klironomos, J.N. 2011. Influence of trees on the spatial structure of arbuscular mycorrhizal communities in a temperate tree-based intercropping system. Agric. Ecosyst. Environ. 144, 13–20.CrossRefGoogle Scholar
  6. Balestrini, R., Magurno, F., Walker, C., Lumini, E., and Bianciotto, V. 2010. Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop. Environ. Microbiol. Rep. 2, 594–604.CrossRefPubMedGoogle Scholar
  7. Blaser, B.C., Gibson, L.R., Singer, J.W., and Jannink, J.L. 2006. Optimizing seeding rates for winter cereal grains and frost-seeded red clover intercrops. Agron. J. 98, 1041–1049.CrossRefGoogle Scholar
  8. Borriello, R., Lumini, E., Girlanda, M., Bonfante, P., and Bianciotto, V. 2012. Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol. Fertil. Soils 48, 911–922.CrossRefGoogle Scholar
  9. Boyetchko, S.M. and Tewari, J.P. 1990. Root colonization of different hosts by the vesicular–arbuscular mycorrhizal fungus Glomus dimorphicum. Plant Soil 129, 131–136.Google Scholar
  10. Bray, R.H. and Kurtz, L.T. 1945 Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–45.CrossRefGoogle Scholar
  11. Brundrett, M., Beegher, N., Dell, B., Groove, T., and Malajczuk, N. 1996. Working with mycorrhizas in Forestry and Agriculture. ACIAR Monograph 32.Google Scholar
  12. Chifflot, V., Rivest, D., Olivier, A., Cogliastro, A., and Khasa, D. 2009. Molecular analysis of arbuscular mycorrhizal community structure and spores distribution in tree-based intercropping and forest systems. Agric. Ecosyst. Environ. 131, 32–39.CrossRefGoogle Scholar
  13. Clark, R.B. and Zeto, S.K. 2000. Mineral acquisition by arbuscular mycorrhizal plants. J. Plant. Nutr. 23, 867–902.CrossRefGoogle Scholar
  14. Daniell, T.J., Husband, R., Fitter, A.H., and Young, J.P.W. 2001. Molecular diversity of arbuscular mycorrhizal fungi colonizing arable crops. FEMS Microbiol. Ecol. 36, 203–209.CrossRefPubMedGoogle Scholar
  15. FAO. 2015. The State of Food Insecurity in the World 2014. Strengthening the enabling environment for food security and nutrition. http://wwwfaoorg/3/a-i4646e.Google Scholar
  16. Giovannetti, M., Azzolini, D., and Citernesi, A.S. 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl. Environ. Microbiol. 65, 5571–5575.PubMedCentralPubMedGoogle Scholar
  17. Giovannetti, M., Fortuna, P., Citernesi, A.S., Morini, S., and Nuti, M.P. 2001. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol. 151, 717–724.CrossRefGoogle Scholar
  18. Giovannetti, M. and Mosse, B. 1980. An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500.CrossRefGoogle Scholar
  19. Giovannetti, M., Schubert, A., Cravero, M.C., and Salutini, L. 1988. Spore production by the vesicular-arbuscular mycorrhizal fungus Glomus monosporum as related to host species, root colonization and plant growth enhancement. Biol. Fertil. Soils 6, 120–124.CrossRefGoogle Scholar
  20. Gollotte, A., van Tuinen, D., and 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.CrossRefPubMedGoogle Scholar
  21. Gosling, P., Mead, A., Proctor, M., Hammond, J.P., and Bending, G.D. 2013. Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol. 198, 546–556.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Hart, M.M., Forsythe, J., Oshowski, B., Bücking, H., Jansa, J., and Kiers, E.T. 2013. Hiding in a crowd–does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis?. Symbiosis 59, 47–56.CrossRefGoogle Scholar
  23. Higo, M., Isobe, K., Drijber, R.A., Kondo, K., Yamaguchi, M., Takeyama, S., Suzuki, Y., Niijima, D., Matsuda, Y., Ishii, R., and 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, 913–926.CrossRefGoogle Scholar
  24. Higo, M., Isobe, K., Kang, D.J., Ujiie, K., Drijber, R.A., and Ishii, R. 2010. Inoculation with arbuscular mycorrhizal fungi or crop rotation with mycorrhizal plants improves the growth of maize in limed acid sulfate soil. Plant Prod. Sci. 13, 74–79.CrossRefGoogle Scholar
  25. Higo, M., Isobe, K., Kondo, T., Yamaguchi, M., Takeyama, S., Drijber, R.A., and Torigoe, Y. 2015a. Temporal variation of the molecular diversity of arbuscular mycorrhizal communities in three different winter cover crop rotational systems. Biol. Fertil. Soils 51, 21–32.CrossRefGoogle Scholar
  26. Higo, M., Isobe, K., Matsuda, Y., Ichida, M., and Torigoe, Y. 2015b. Influence of sowing season and host crop identity on the community structure of arbuscular mycorrhizal fungi colonizing roots of two different gramineous and leguminous crop species. Adv. Microbiol. 5, 107–116.CrossRefGoogle Scholar
  27. Higo, M., Isobe, K., Yamaguchi, M., Drijber, R.A., and Ishii, R. 2013. Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems. Biol. Fertil. Soils 49, 1085–1096.CrossRefGoogle Scholar
  28. Higo, M., Isobe, K., Yamaguchi, M., and Torigoe, Y. 2015c. Impact of a soil sampling strategy on the spatial distribution and diversity of arbuscular mycorrhizal communities at a small scale in two winter cover crop rotational systems. Ann. Microbiol. 65, 985–993.CrossRefGoogle Scholar
  29. Holland, T.C., Bowen, P., Bogdanoff, C., and Hart, M.M. 2014. How distinct are arbuscular mycorrhizal fungal communities associating with grapevines? Biol. Fertil. Soils 50, 667–674.CrossRefGoogle Scholar
  30. Isobe, K., Higo, M., Kondo, T., Sato, N., Takeyama, S., and Torigoe, Y. 2014. Effect of winter crop species on arbuscular mycorrhizal fungal colonization and subsequent soybean yields. Plant Prod. Sci. 17, 260–267.CrossRefGoogle Scholar
  31. Isobe, K., Maruyama, K., Nagai, S., Higo, M., Maekawa, T., Mizonobe, G., Drijber, R.A., and Ishii, R. 2011. Arbuscular mycorrhizal fungal community structure in soybean roots: Comparison between Kanagawa and Hokkaido, Japan. Adv. Microbiol. 1, 13–22.CrossRefGoogle Scholar
  32. Isobe, K. and Tsuboki, Y. 1998. The Relationship between growth promotion by arbuscular mycorrhizal fungi and root morphology and phosphorus absorption in gramineousand leguninous groups. Jpn. J. Crop Sci. 67, 347–352.CrossRefGoogle Scholar
  33. Jansa, J., Erb, A., Oberholzer, H.R., Šmilauer, P., and 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.CrossRefPubMedGoogle Scholar
  34. Jansa, J., Smith, F.A., and Smith, S.E. 2008. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi?. New Phytol. 177, 779–789.CrossRefPubMedGoogle Scholar
  35. Jemo, M., Souleymanou, A., Frossard, E., and Jansa, J. 2014. Cropping enhances mycorrhizal benefits to maize in a tropical soil. Soil Biol. Biochem. 79, 117–124.CrossRefGoogle Scholar
  36. Kaspar, T.C., Radke, J.K., and Laflen, J.M. 2001. Small grain cover crops and wheel traffic effects on infiltration, runoff and erosion. J. Soil Water Conserv. 56, 160–164.Google Scholar
  37. Karasawa, T. and Takebe, M. 2012. Temporal or spatial arrangements of cover crops to promote arbuscular mycorrhizal colonization and P uptake of upland crops grown after nonmycorrhizal crops. Plant Soil 353, 355–366.CrossRefGoogle Scholar
  38. Knegt, B., Jansa, J., Franken, O., Engelmoer, D.J., Werner, G.D., Bücking, H., and Kiers, E.T. 2015. Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol. DOI:10.1016/jfuneco.2014.09.011.Google Scholar
  39. Lekberg, Y., Schnoor, T., Kjøller, R., Gibbons, S.M., Hansen, L.H., Al-Soud, W.A., Sorensen, S.J., and Rosendahl, S. 2012. 454-Sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J. Ecol. 100, 151–160.CrossRefGoogle Scholar
  40. Lendenmann, M., Thonar, C., Barnard, R.L., Salmon, Y., Werner, R.A., Frossard, E., and Jansa, J. 2011. Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21, 689–702.CrossRefPubMedGoogle Scholar
  41. Mummey, D.L. and Rillig, M.C. 2008. Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiol. Ecol. 64, 260–270.CrossRefPubMedGoogle Scholar
  42. Njeru, E.M., Avio, L., Sbrana, C., Turrini, A., Bocci, G., Bàrberi, P., and Giovannetti, M. 2014. First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron. Sustain. Dev. 34, 841–848.CrossRefGoogle Scholar
  43. Oehl, F., Sieverding, E., Ineichen, K., Mäder, P., Boller, T., and 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, 2816–282.PubMedCentralCrossRefPubMedGoogle Scholar
  44. Oka, N., Karasawa, T., Okazaki, K., and Takebe, M. 2010. Maintenance of soybean yield with reduced phosphorus application by previous cropping with mycorrhizal plants. Soil Sci. Plant Nutr. 56, 824–830.CrossRefGoogle Scholar
  45. Öpik, M., Zobel, M., Cantero, J.J., Davison, J., Facelli, J.M., Hiiesalu, I., Jairus, T., Kalwij, J.M., Koorem, K., Leal, M.E., et al. 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23, 411–430.CrossRefPubMedGoogle Scholar
  46. Parkin, T.B., Kaspar, T.C., and Singer, J.W. 2006. Cover crop effects on the fate of N following soil application of swine manure. Plant Soil 289, 141–152.CrossRefGoogle Scholar
  47. Phillips, J.M. and Hayman, D.S. 1970. Improved procedures for clearing roots and staining parasitic vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–160.CrossRefGoogle Scholar
  48. Reicosky, D.C. and Forcella, F. 1998. Cover crops and soil quality interactions in agroecosystems. J. Soil Water Conserv. 53, 224–229.Google Scholar
  49. Renker, C., Weißhuhn, K., Kellner, H., and Buscot, F. 2006. Rationalizing molecular analysis of field-collected roots for assessing diversity of arbuscular mycorrhizal fungi: to pool, or not to pool, this is the question. Mycorrhiza 16, 525–531.CrossRefPubMedGoogle Scholar
  50. Rillig, M.C. and Field, C.B. 2003. Arbuscular mycorrhizae respond to plants exposed to elevated atmospheric CO2 as a function of soil depth. Plant Soil 254, 383–391.CrossRefGoogle Scholar
  51. Ryder, M.H. and Fares, A. 2008. Evaluating cover crops (Sudex, Sunn Hemp, Oats) for use as vegetative filters to control sediment and nutrient loading from agricultural runoff in a Hawaiian watershed. J. Am. Water Resour. As. 44, 640–653.CrossRefGoogle Scholar
  52. Sa, T.M. and Israel, D.W. 1995. Nitrogen assimilation in nitrogenfixing soybean plants during phosphorus deficiency. Crop Sci. 35, 814–820.CrossRefGoogle Scholar
  53. Smith, S.E. and Read, D.J. 2008. Arbuscular mycorrhizaes, pp. 13–187. In Smith, S.E. and Read, D.J. (eds), Mycorrhizal symbiosis 3rd Edition. Academic Press, London, UK.Google Scholar
  54. Taffouo, V.D., Ngwene, B., Akoa, A., and Franken, P. 2014. Influence of phosphorus application and arbuscular mycorrhizal inoculation on growth, foliar nitrogen mobilization, and phosphorus partitioning in cowpea plants. Mycorrhiza 24, 361–368.CrossRefPubMedGoogle Scholar
  55. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.PubMedCentralCrossRefPubMedGoogle Scholar
  56. Tennant, D. 1975. A test of a modified line intersect method of estimating root length. J. Ecol. 63, 995–1001.CrossRefGoogle Scholar
  57. ter Braak, C. and Šmilauer, P. 2002. CANOCO reference manual and Canodraw for Windows user's guide: Software for canonical community ordination, 4.5 (Ed). Microcomputer Power, Ithaca.Google Scholar
  58. Thonar, C., Frossard, E., Smilauer, P., and Jansa, J. 2014. Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. Mol. Ecol. 23, 733–746.CrossRefPubMedGoogle Scholar
  59. Thonar, C., Schnepf, A., Frossard, E., Roose, T., and Jansa, J. 2011. Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339, 231–245.CrossRefGoogle Scholar
  60. Thorup-Kristensen, K., Dresboll, D.B., and Kristensen, H.L. 2012. Crop yield, root growth, and nutrient dynamics in a conventional and three organic cropping systems with different levels of external inputs and N re-cycling through fertility building crops. Euro. Agron. J. 37, 66–82.CrossRefGoogle Scholar
  61. Trouvelot, S., van Tuinen, D., Hijri, M., and Gianinazzi-Pearson, V. 1999. Visualization of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hyhridization. Mycorrhiza 8, 203–206.CrossRefGoogle Scholar
  62. Tsuji, H., Yamamoto, H., Matsuo, K., and Usuki, K. 2002. Effects of no-tillage on the root system development of groundnut, maize and soybean in Andosol. Root Research 2, 43–4.CrossRefGoogle Scholar
  63. van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., and Sanders, E.R. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72.CrossRefGoogle Scholar
  64. van Tuinen, D., Jacquot, E., Zhao, B., Gollotte, A., and Gianinazzi-Pearson, V. 1998. Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol. Ecol. 7, 879–887.CrossRefPubMedGoogle Scholar
  65. Wolfe, B.E., Mummey, D.L., Rillig, M.C., and Klironomos, J.N. 2007. Small-scale spatial heterogeneity of arbuscular mycorrhizal fungal abundance and community composition in a wetland plant community. Mycorrhiza 17, 175–183.CrossRefPubMedGoogle Scholar
  66. Yang, H., Zang, Y., Yuan, Y., Tang, J., and 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.PubMedCentralCrossRefPubMedGoogle Scholar
  67. Yasuda, K., Fujii, Y., and Shibuya, T. 1987. Difference of plants growth and phosphorus uptake at low phosphorus condition. Jpn. Soil Sci. Plant Nutri. 58, 180–186.Google Scholar
  68. Yoneyama, T., Horie, H., Takebe, M., and Tanno, F. 1990. Absorption of phosphorus from soil by crops: ii. the relationship between root mass and phosphorus absorption. Jpn. Soil Sci. Plant Nutri. 61, 382–385.Google Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Masao Higo
    • 1
  • Katsunori Isobe
    • 1
  • Yusuke Miyazawa
    • 1
  • Yukiya Matsuda
    • 1
  • Rhae A. Drijber
    • 2
  • Yoichi Torigoe
    • 1
  1. 1.College of Bioresource SciencesNihon UniversityKanagawaJapan
  2. 2.Department of Agronomy and HorticultureUniversity of Nebraska-LincolnLincolnUSA

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