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The arbuscular mycorrhizal symbiosis links N mineralization to plant demand

Mycorrhiza volume 19, pages 239–246 (2009)Cite this article

Abstract

Arbuscular mycorrhizal (AM) fungi facilitate inorganic N (NH4 + or NO3 −) uptake by plants, but their role in N mobilization from organic sources is unclear. We hypothesized that arbuscular mycorrhizae enhance the ability of a plant to use organic residues (ORs) as a source of N. This was tested under controlled glasshouse conditions by burying a patch of OR in soil separated by 20-μm nylon mesh so that only fungal hyphae can pass through it. The fate of the N contained in the OR patch, as influenced by Glomus claroideum, Glomus clarum, or Glomus intraradices over 24 weeks, was determined using 15N as a tracer. AM fungal species enhanced N mineralization from OR to different levels. N recovery and translocation to Russian wild rye by hyphae reached 25% of mineralized N in G. clarum, which was most effective despite its smaller extraradical development in soil. Mobilization of N by G. clarum relieved plant N deficiency and enhanced plant growth. We show that AM hyphae modify soil functioning by linking plant growth to N mineralization from OR. AM species enhance N mineralization differentially leading to species-specific changes in the quality of the soil environment (soil C-to-N ratio) and structure of the soil microbial community.

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References

  • Abuzinadah RA, Read DJ (1989) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. V. Nitrogen transfer in birch (Betula pendula) grown in association with mycorrhizal and non-mycorrhizal fungi. New Phytol 112:61–68. doi:10.1111/j.1469-8137.1989.tb00309.x

    CAS  Article  Google Scholar 

  • Andrade G (2004) Role of functional groups of microorganisms on the rhizosphere microcosm dynamics. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Germany, pp 51–71

    Google Scholar 

  • Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192:71–79. doi:10.1023/A:1004249629643

    CAS  Article  Google Scholar 

  • Aneja M, Sharma S, Fleischmann F, Stich S, Heller W, Bahnweg G, Munch J, Schloter M (2006) Microbial colonization of beech and spruce litter—influence of decomposition site and plant litter species on the diversity of microbial community. Microb Ecol 52:127–135. doi:10.1007/s00248-006-9006-3

    Article  PubMed  Google Scholar 

  • Aristizábal C, Rivera EL, Janos DP (2004) Arbuscular mycorrhizal fungi colonize decomposing leaves of Myrica parvifolia, M. pubescens and Paepalanthus sp. Mycorrhiza 14:221–228. doi:10.1007/s00572-003-0259-0

    Article  PubMed  Google Scholar 

  • Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361:150–153. doi:10.1038/361150a0

    CAS  Article  Google Scholar 

  • Dalpé Y, Hamel C (2008) Vesicular-arbuscular mycorrhiza. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, Boca Raton, pp 287–302

    Google Scholar 

  • Garcia Romera I, Garcia Garrido JM, Ocampo JA (1991) Pectolytic enzymes in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. FEMS Microbiol Lett 78:343–346. doi:10.1111/j.1574-6968.1991.tb04467.x

    CAS  Article  Google Scholar 

  • Garcia-Garrido JM, Garcia-Romera I, Ocampo JA (1992) Cellulase production by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.). Gerd Trappe. New Phytol 121:221–226. doi:10.1111/j.1469-8137.1992.tb01107.x

    CAS  Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823. doi:10.1038/nature03610

    CAS  Article  PubMed  Google Scholar 

  • Ha K, Marschner P, Bünemann E (2008) Dynamics of C, N, P and microbial community composition in particulate soil organic matter during residue decomposition. Plant Soil 303:253–264. doi:10.1007/s11104-007-9504-1

    CAS  Article  Google Scholar 

  • Hamel C (2004) Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Can J Soil Sci 84:383–395

    CAS  Article  Google Scholar 

  • Hamel C, Hanson K, Selles F, Cruz AF, Lemke R, McConkey B, Zentner R (2006) Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie. Soil Biol Biochem 38:2104–2116. doi:10.1016/j.soilbio.2006.01.011

    CAS  Article  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285. doi:10.1023/A:1026500810385

    CAS  Article  Google Scholar 

  • Hodge A (2003a) N capture by Plantago lanceolata and Brassica napus from organis material: The influence of spatial dispersion, plant competition and an arbuscular mycorrhizal fungus. J Exp Bot 57:401–411. doi:10.1093/jxb/eri280

    Article  Google Scholar 

  • Hodge A (2003b) Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytol 157:303–314. doi:10.1046/j.1469-8137.2003.00662.x

    Article  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299. doi:10.1038/35095041

    CAS  Article  PubMed  Google Scholar 

  • Huberty CJ (1994) Applied discriminant analysis. Wiley, New York, p 466

    Google Scholar 

  • Jackson LE, Burger M, Cavagnaro TR (2008) Nitrogen transformations and ecosystem services. Annu Rev Plant Biol 59:341–363. doi:10.1146/annurev.arplant.59.032607.092932

    CAS  Article  PubMed  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1994) Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels. Plant Soil 160:1–9. doi:10.1007/BF00150340

    CAS  Article  Google Scholar 

  • Jones DL, Darrah PR (1992) Re-sorption of organic components by roots of Zea mays L. and its consequences in the rhizosphere. Plant Soil 143:259–266. doi:10.1007/BF00007881

    CAS  Article  Google Scholar 

  • Kawashima H, Konzaki N, Kobayashi M, Shimizu S (1996) Biosynthesis of trans fatty acids in a fungus Cladosporium sphaerospermium and some bacteria isolated from fish viscera. Biosci Biotechnol Biochem 60:1888–1890

    CAS  Article  Google Scholar 

  • Koske RE, Gemma JN (2000) A modified procedure for staining roots to detect AM mycorrhizas. Mycol Res 92:486–489

    Article  Google Scholar 

  • Leake JR, Read DJ (1990) Proteinase activity in mycorrhizal fungi. II. The effects of mineral and organic nitrogen sources on induction of extracellular proteinase in Hymenoscyphus ericae (Read) Korf & Kernan. New Phytol 116:123–128. doi:10.1111/j.1469-8137.1990.tb00517.x

    CAS  Article  Google Scholar 

  • Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543. doi:10.1111/j.1469-8137.2006.01846.x

    CAS  Article  PubMed  Google Scholar 

  • Lioussanne L, Beauregard MS, Hamel C, Jolicoeur M, St-Arnaud M (2008) Interactions between arbuscular mycorrhiza and soil microorganisms. In: Khasa D, Piché Y, Coughlan A (eds) Advances in mycorrhizal science and technology. NRC, Ottawa

    Google Scholar 

  • Liu A, Hamel C, Hamilton R, Smith D (2000) Mycorrhizae formation and nutrient uptake of new corn (Zea mays L.) hybrids with extreme canopy and leaf architecture as influenced by soil N and P levels. Plant Soil 221:157–166. doi:10.1023/A:1004777821422

    CAS  Article  Google Scholar 

  • Liu A, Plenchette C, Hamel C (2007) Soil nutrient and water providers: How arbuscular mycorrhizal mycelia support plant performance in a resource-limited world. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production. Haworth, Binghamton, pp 38–66

    Google Scholar 

  • Mader P, Vierheilig H, Streitwolf-Engel R, Boller T, Frey B, Christie P, Wiemken A (2000) Transport of 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146:155–161. doi:10.1046/j.1469-8137.2000.00615.x

    Article  Google Scholar 

  • Marschner P, Crowley D, Lieberei R (2001) Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize. Mycorrhiza 11:297–302. doi:10.1007/s00572-001-0136-7

    CAS  Article  PubMed  Google Scholar 

  • Marschner P, Crowley DE (1996a) Physiological activity of a bioluminescent Pseudomonas fluorescens (strain 2–79) in the rhizosphere of mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.). Soil Biol Biochem 28:869–876. doi:10.1016/0038-0717(96)00072-7

    CAS  Article  Google Scholar 

  • Marschner P, Crowley DE (1996b) Root colonization of mycorrhizal and non-mycorrhizal pepper (Capsicum annuum) by Pseudomonas fluorescens 2-79RL. New Phytol 134:115–122. doi:10.1111/j.1469-8137.1996.tb01151.x

    Article  Google Scholar 

  • Milbury WF, Stack VT, Doll FL (1970) Simultaneous determination of total phosphorus and total Kjeldahl nitrogen in activated sludge with the Technicon continuous digestor system. In: Technicon International Congress, Advances in Automatic Analysis, Industrial Analysis, pp. 299–304

  • Nakano A, Takahashi K, Kimura M (1999) The carbon origin of arbuscular mycorrhizal fungi estimated from δ13C values of individual spores. Mycorrhiza 9:41–47. doi:10.1007/s005720050261

    CAS  Article  Google Scholar 

  • Newman EI (1966) A method for estimating total length of root in a sample. J Appl Ecol 3:139–145. doi:10.2307/2401670

    Article  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. doi:10.1016/S0169-5347(00)89157-0

    CAS  Article  PubMed  Google Scholar 

  • Noel RJ, Hambleton LG (1976) Collaborative study of a semi-automated method for the determination of crude protein in animal feeds. J Assoc Off Anal Chem 59:134–140

    CAS  PubMed  Google Scholar 

  • Petersen SO, Klug MJ (1994) Effects of sieving, storage, and incubation temperature on the phospholipid fatty acid profile of a soil microbial community. Appl Environ Microbiol 60:2421–2430

    CAS  PubMed  PubMed Central  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124. doi:10.1007/BF00202343

    CAS  Article  Google Scholar 

  • Ravnskov S, Nybroe OLE, Jakobsen I (1999) Influence of an arbuscular mycorrhizal fungus on Pseudomonas fluorescens DF57 in rhizosphere and hyphosphere soil. New Phytol 142:113–122. doi:10.1046/j.1469-8137.1999.00374.x

    Article  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391. doi:10.1007/BF01972080

    Article  Google Scholar 

  • Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97

    CAS  Article  PubMed  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563. doi:10.1016/S0038-0717(03)00015-4

    CAS  Article  Google Scholar 

  • Secilia J, Bagyaraj DJ (1987) Bacteria and actinomycetes associated with pot cultures of vesicular–arbuscular mycorrhizas. Can J Microbiol 33:1069–1073

    Article  Google Scholar 

  • Spring S, Schulze R, Overmann J, Schleifer KH (2000) Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studies. FEMS Microbiol Rev 24:573–590. doi:10.1111/j.1574-6976.2000.tb00559.x

    CAS  Article  PubMed  Google Scholar 

  • St. John TV, Coleman DC, Reid CPP (1983) Association of vesicular–arbuscular mycorrhizal hyphae with soil organic particles. Ecology 64:957–959. doi:10.2307/1937216

    Article  Google Scholar 

  • Stanton NL (1988) The Underground in Grasslands. Annu Rev Ecol Syst 19:573–589. doi:10.1146/annurev.es.19.110188.003041

    Article  Google Scholar 

  • Sundh I, Nilsson M, Borga P (1997) Variation in microbial community structure in two boreal peatlands as determined by analysis of phospholipid fatty acid profiles. Appl Environ Microbiol 63:1476–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963. doi:10.1111/j.1365-2435.2008.01402.x

    Article  Google Scholar 

  • Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254. doi:10.1111/j.1365-3040.2005.01360.x

    CAS  Article  Google Scholar 

  • Tinker PBH, Nye PH (2000) Solute transport in the rhizosphere. Oxford Univ. Press, Oxford

    Google Scholar 

  • Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304. doi:10.1111/j.1574-6941.2007.00337.x

    CAS  Article  PubMed  Google Scholar 

  • Varley JA (1966) Automated method for the determination of nitrogen, phosphorus and potassium in plant material. Analyst (Lond) 91:119–126. doi:10.1039/an9669100119

    CAS  Article  Google Scholar 

  • Varma A (1999) Hydrolytic enzymes from arbuscular mycorrhizae: the current status. In: Varma A, Hock B (eds) Mycorrhiza, 2nd edn. Springer, Berlin, pp 373–389

    Chapter  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr. Yolande Dalpé for providing the AM fungal species. This work was supported by a grant from AAFC-GAPS #348.

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Affiliations

  1. Semiarid Prairie Agricultural Research Centre, Agriculture and Agri-Food Canada, P.O. Box 1030, 1 Airport Rd., Swift Current, Saskatchewan, S9H 3X2, Canada

    A. Atul-Nayyar, C. Hamel & K. Hanson

  2. Department of Soil Science, University of Saskatchewan, 51 Campus Drive, Saskatoon, SK, S7N 5A8, Canada

    A. Atul-Nayyar, C. Hamel & J. Germida

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  1. A. Atul-Nayyar
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  2. C. Hamel
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  3. K. Hanson
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  4. J. Germida
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Correspondence to C. Hamel.

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Atul-Nayyar, A., Hamel, C., Hanson, K. et al. The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19, 239–246 (2009). https://doi.org/10.1007/s00572-008-0215-0

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  • DOI: https://doi.org/10.1007/s00572-008-0215-0

Keywords

  • Arbuscular mycorrhizal fungi
  • Organic residue decomposition
  • N mineralization
  • N mobilization
  • Soil microbial community composition