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The Role of Mycorrhiza in Transformation of Nitrogen Compounds in Soil and Nitrogen Nutrition of Plants: A Review

  • SOIL BIOLOGY
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Abstract

The role of mycorrhizal symbiosis as a control of the biogeochemical cycle of nitrogen in soils and in the nitrogen nutrition of plants is considered. The contribution of ericoid mycorrhiza (ErM) and ectomycorrhiza (EcM) to nitrogen (N) supply of host plants is well known, whereas the role of arbuscular mycorrhiza (ArM) is insufficiently understood. Exoenzymes released into the soil from the ErM and EcM mycelium favor the hydrolysis of high-molecular-weight N-containing organic compounds of plant litter and soils to \({\text{NH}}_{4}^{ + }\) or amino acids that are then transported toward plant roots and are absorbed by them. ArM-producing fungi have a limited capacity to release hydrolytic enzymes capable to decompose high-molecular-weight organic compounds into the soil (or do not have it at all). Therefore, they are specialized on the absorption of inorganic forms of N and amino acids appearing in the soil in the course of decomposition of high-molecular-weight N-containing compounds by saprotrophic microorganisms. The activity of hydrolytic exoenzymes and the role of mycorrhiza in the nitrogen nutrition of plants become more significant under conditions of the low supply with mineral N compounds and decrease upon the rise in availability of mineral N compounds. At the same time, mycorrhizal fungi and host plants may compete for the limited resource. The isotopic composition of N in plants (δ15N) and the fractionation of 15N isotope between the mycorrhizal fungi and host plants are considered indicative of the participation of mycorrhiza in the nitrogen nutrition of plants.

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REFERENCES

  1. A. A. Betekhtina, T. A. Mukhacheva, S. Yu. Kovalev, A. P. Gusev, and D. V. Veselkin, “Abundance and diversity of arbuscular mycorrhizal fungi in invasive Solidago canadensis and indigenous S. virgaurea,” Russ. J. Ecol. 47, 575–579 (2016).

    Article  Google Scholar 

  2. D. V. Veselkin, N. V. Lukina, and T. S. Chibrik, “The ratio of mycorrhizal and nonmycorrhizal plant species in primary technogenic successions,” Russ. J. Ecol. 46, 417–424 (2015).

    Article  Google Scholar 

  3. D. V. Veselkin, E. F. Markovskaya, A. A. Betekhina, A. V. Sonina, and L. A. Sergienko, “Mycorrhiza formation in vascular plants of the western coast of the White Sea,” Uch. Zap. Petrozavodsk. Gos. Univ., No. 8, 20–26 (2016).

  4. N. G. Lavrenov, A. S. Zernov, A. M. Kipkeev, D. K.  Tekeev, R. B. Semenova, A. A. Akhmetzhanova, L. G. Perevedentseva, N. A. Sudzilovskaya, M. Yu. Korneecheva, and V. G. Onipchenko, “Plant mycorrhiza under extreme conditions of snow beds Alpine communities in Armenia,” Biol. Bull. Rev. 8, 401–405 (2018).

    Article  Google Scholar 

  5. M. I. Makarov, “The nitrogen isotopic composition in soils and plants: its use in environmental studies (a review),” Eurasian Soil Sci. 42, 1335–1347 (2009).

    Article  Google Scholar 

  6. V. F. Malysheva, E. F. Malysheva, E. Yu. Voronina, A. G. Fedoseeva, N. M. Bibikov, D. S. Kiseleva, A. V. Tiunov, and A. E. Kovalenko, “Mycorrhiza of Pyroleae species (Pyrola rotundifolia, P. media, and Orthilia secunda): composition of fungal symbionts and trophic status of the plants,” Mikol. Fitopatol. 51 (6), 350–364 (2017).

    Google Scholar 

  7. O. V. Menyailo, A. I. Matvienko, A. L. Stepanov, and M. I. Makarov, “Measuring soil CO2 efflux: effect of collar depth,” Russ. J. Ecol. 46, 152–156 (2015).

    Article  Google Scholar 

  8. S. E. Smith and D. J. Read, Mycorrhizal Symbiosis (Elsevier, Amsterdam, 2008; KMK, Moscow, 2012).

  9. A. P. Yurkov, G. V. Stepanova, L. M. Yakobi, A. P. Kozhemyakov, N. Kh. Sergaliev, R. K. Amenova, R. Sh. Dzhaparov, M. A. Volodin, A. S. Tlepanov, and E. N. Baimukanov, “Productivity of spring and winter wheat using a fungus with arbuscular mycorrhiza Glomus intraradices in conditions of moisture deficiency,” Kormoproizvodstvo, No. 11, 18–20 (2012).

    Google Scholar 

  10. A. P. Yurkov, L. M. Yakobi, N. I. Dzyubenko, M. F. Shishova, N. A. Provorov, A. P. Kozhemyakov, and A. A. Zavalin, “Polymorphism of population of black medick variety Pavlovskaya by productivity mycorrhization, and efficiency of symbiosis with Glomus intraradices,” S-kh. Biol., No. 3, 65–70 (2011).

  11. C. Averill and A. Finzi, “Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N,” Ecology 92, 883–891 (2011).

    Article  Google Scholar 

  12. C. Averill, B. L. Turner, and A. C. Finzi, “Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage,” Nature 505, 543–546 (2014).

    Article  Google Scholar 

  13. G. R. Azcón-Aguilar, L. L. Handley, and C. M. Scrimgeour, “The δ15N of lettuce and barley are affected by AM status and external concentration of N,” New Phytol. 138, 19–26 (1998).

    Article  Google Scholar 

  14. S. F. Bender, F. Conen, and M. G. A. van der Heijden, “Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland,” Soil Biol. Biochem. 80, 283–292 (2015).

    Article  Google Scholar 

  15. G. J. Bethlenfalvay, M. S. Brown, and R. S. Pacovsky, “Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: development of the host plant,” Phytopathology 72, 889–893 (1982).

    Article  Google Scholar 

  16. I. T. M. Bödeker, K. E. Clemmensen, W. Boer, F. Martin, E. Olson, and B. D. Lindahl, “Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems,” New Phytol. 203, 245–256 (2014).

    Article  Google Scholar 

  17. E. R. Brzostek, A. Greco, J. E. Drake, and A. C. Finzi, “Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils,” Biogeochemistry 115, 65–76 (2013).

    Article  Google Scholar 

  18. D. D. Cameron and J. F. Bolin, “Isotopic evidence of partial mycoheterotrophy in the Gentianaceae: Bartonia virginica and Obolaria virginica as case studies,” Am. J. Bot. 97, 1272–1277 (2010).

    Article  Google Scholar 

  19. K. E. Clemmensen, R. D. Finlay, A. Dahlberg, J. Stenlid, D. A. Wardle, and B. D. Lindahl, “Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests,” New Phytol. 205, 1525–1536 (2015).

    Article  Google Scholar 

  20. F. S. Chapin, P. M. Vitousek, and K. Vancleve, “The nature of nutrient limitation in plant-communities,” Am. Nat. 127, 48–58 (1986).

    Article  Google Scholar 

  21. A. Corrêa, C. Cruz, and N. Ferrol, “Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown,” Mycorrhiza 25, 499–515 (2015).

    Article  Google Scholar 

  22. P.-E. Courty, M. Buée, A. G. Diedhiou, P. Frey-Klett, F. Le Tacon, F. Rineau, M.-P. Turpault, S. Uroz, and Garbaye, J. “The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts,” Soil Biol. Biochem. 42, 679–698 (2010).

    Article  Google Scholar 

  23. P.-E. Courty, F. Walder, T. Boller, K. Ineichen, A. Wiemken, A. Rousteau, and M.-A. Selosse, “Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis,” Plant Physiol. 156, 952–961 (2011).

    Article  Google Scholar 

  24. P.-E. Courty, P. Doubkov, S. Calabrese, H. Niemann, M. F. Lehmann, M. Vosatka, and M.-A. Selosse “Species-dependent partitioning of C and N stable isotopes between arbuscular mycorrhizal fungi and their C3 and C4 hosts,” Soil Biol. Biochem. 82, 52–61 (2015).

    Article  Google Scholar 

  25. J. M. Craine, A. J. Elmore, M. P. M. Aidar, M. Bustamante, T. E. Dawson, E. A. Hobbie, A. Kahmen, M. C. Mack, K. K. McLauchlan, A. Michelsen, G. B. Nardoto, L. H. Pardo, J. Peñuelas, P. B. Reich, E. A. G. Schuur, et al., “Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability,” New Phytol. 183, 980–992 (2009).

    Article  Google Scholar 

  26. J. M. Craine, W. G. Lee, W. J. Bond, R. J. Williams, and L. C. Johnson, “Environmental constraints on a global relationship among leaf and root traits of grasses,” Ecology 86, 12–19 (2005).

    Article  Google Scholar 

  27. T. E. Dawson, S. Mambelli, A. H. Plamboeck, P. H. Templer, and K. P. Tu, “Stable isotopes in plant ecology,” Annu. Rev. Ecol. Syst. 33, 507–559 (2002).

    Article  Google Scholar 

  28. P. Dijkstra, C. Williamson, O. Menyailo, R. Doucett, G. Koch, and B. A. Hungate, “Nitrogen stable isotope composition of leaves and roots of plants growing in a forest and a meadow,” Isotopes Environ. Health Stud. 39, 29–39 (2003).

    Article  Google Scholar 

  29. M. Ellström, “Effects of nitrogen deposition on the growth, metabolism and activity of ectomycorrhizal fungi”, PhD Thesis (Lund University, Lund, 2014).

  30. K. S. Emmerton, T. V. Callaghan, H. E. Jones, J. R. Leake, A. Michelsen, and D. J. Read, “Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi,” New Phytol. 151, 503–511 (2001).

    Article  Google Scholar 

  31. P. Etcheverría, D. Huygens, R. Godoy, F. Borie, and P. Boeckx, “Arbuscular mycorrhizal fungi contribute to 13C and 15N enrichment of soil organic matter in forest soils,” Soil Biol. Biochem. 41, 858–861 (2009).

    Article  Google Scholar 

  32. R. D. Evans, A. J. Bloom, S. S. Sukrapanna, and J. R. Ehleringer, “Nitrogen isotope composition of tomato (Lucopersicon esculentum Mill. Cv. T-5) grown under ammonium or nitrate nutrition,” Plant Cell Environ. 19, 1317–1323 (1996).

    Article  Google Scholar 

  33. C. R. Fellbaum, E. W. Gachomo, Y. Beesetty, S. Choudhari, G. D. Strahan, P. E. Pfeffer, E. T. Kiers, and H. Bucking, “Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis,” Proc. Natl. Acad. Sci. U.S.A. 109, 2666–2671 (2012).

    Article  Google Scholar 

  34. O. Franklin, T. Nösholm, P. Högberg, and M. N. Högberg, “Forests trapped in nitrogen limitation—an ecological market perspective on ectomycorrhizal symbiosis,” New Phytol. 203, 657–666 (2014).

    Article  Google Scholar 

  35. A. Gallet-Budynek, E. Brzostek, V. L. Rodgers, J. M. Talbot, S. Hyzy, and A. C. Finzi, “Intact amino acid uptake by northern hardwood and conifer trees,” Oecologia 160, 129–138 (2009).

    Article  Google Scholar 

  36. M. Govindarajulu, P. E. Pfeffer, H. Jin, J. Abubaker, D. D. Douds, J. W. Allen, H. Bücking, P. J. Lammers, and Y. Shachar-Hill, “Nitrogen transfer in the arbuscular mycorrhizal symbiosis,” Nature 435, 819–823 (2005).

    Article  Google Scholar 

  37. M. G. A. van der Heijden and T. R. Horton, “Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems,” J. Ecol. 97, 1139–1150 (2009).

    Article  Google Scholar 

  38. M. G. A. van der Heijden, F. M. Martin, M.-A. Selosse, and I. R. Sanders, “Mycorrhizal ecology and evolution: the past, the present, and the future,” New Phytol. 205, 1406–1423 (2015).

    Article  Google Scholar 

  39. M. R. Henn and I. H. Chapela, “Ecophysiology of 13C and 15N isotopic fractionation in forest fungi and the roots of the saprotrophic-mycorrhizal divide,” Oecologia 128, 480–487 (2001).

    Article  Google Scholar 

  40. C. M. Hepper, “A colorimetric method for estimating vesicular-arbuscular mycorrhizal infection in roots,” Soil Biol. Biochem. 9, 15–18 (1977).

    Article  Google Scholar 

  41. E. A. Hobbie and J. V. Colpaert, “Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants,” New Phytol. 157, 115–126 (2003).

    Article  Google Scholar 

  42. J. E. Hobbie and E. A. Hobbie, “N-15 in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra,” Ecology 87, 816–822 (2006).

    Article  Google Scholar 

  43. J. E. Hobbie and P. Högberg, “Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics,” New Phytol. 196, 367–382 (2012).

    Article  Google Scholar 

  44. E. A. Hobbie, A. Jumpponen, and J. Trappe, “Foliar and fungal 15N : 14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models,” Oecologia 146, 258–268 (2005).

    Article  Google Scholar 

  45. E. A. Hobbie, S. A. Macko, and H. H. Shugart, “Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence,” Oecologia 118, 353–360 (1999).

    Article  Google Scholar 

  46. E. A. Hobbie, S. A. Macko, and M. Williams, “Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions,” Oecologia 122, 273–283 (2000).

    Article  Google Scholar 

  47. A. Hodge, C. D. Campbell, and A. H. Fitter, “An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material,” Nature 413, 297–299 (2001).

    Article  Google Scholar 

  48. A. Hodge and A. H. Fitter, “Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling,” Proc. Natl. Acad. Sci. U.S.A. 107, 13754–13759 (2010).

    Article  Google Scholar 

  49. A. Hodge and K. Storer, “Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems,” Plant Soil 386, 1–19 (2015).

    Article  Google Scholar 

  50. M. N. Högberg and P. Högberg, “Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces together with associated roots, half the dissolved organic carbon in a forest soil,” New Phytol. 154, 791–795 (2002).

    Article  Google Scholar 

  51. P. Högberg and I. J. Alexander, “Roles of root symbioses in African woodland and forest: evidence from 15N abundance and foliar analysis,” J. Ecol. 83, 217–224 (1995).

    Article  Google Scholar 

  52. P. Högberg, M. N. Högberg, M. E. Quist, A. Ekblad, and T. Näsholm, “Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris,” New Phytol. 142, 569–576 (1999).

    Article  Google Scholar 

  53. M. D. Jones, F. Grenon, H. Peat, M. Fitzgerald, L. Holt, L. J. Philip, and R. Bradley, “Differences in 15N uptake amongst spruce seedlings colonized by three pioneer ectomycorrhizal fungi in the field,” Fungal Ecol. 2, 110–120 (2009).

    Article  Google Scholar 

  54. A. Kohzu, T. Yoshioka, T. Ando, M. Takahashi, K. Koba, and E. Wada, “Natural 13C and 15N abundance of field-collected fungi and their ecological implications,” New Phytol. 144, 323–334 (1999).

    Article  Google Scholar 

  55. T. E. C. Kraus, R. A. Dahlgren, and R. J. Zasoski, “Tannins in nutrient dynamics of forest ecosystems—a review,” Plant Soil 256, 41–66 (2003).

    Article  Google Scholar 

  56. Legume nitrogen fixation in soils with low phosphorus availability: Adaptation and regulatory implication, Eds. by S. Sulieman, L.P. Tran (Springer, 2017).

  57. R. Liese, T. Lübbe, N. W. Albers, and I. C. Meier, “The mycorrhizal type governs root exudation and N uptake of temperate tree species,” Tree Physiol. 38, 83–95 (2017).

    Article  Google Scholar 

  58. E. A. Lilleskov, E. A. Hobbie, and T. J. Fahey, “Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes,” New Phytol. 154, 219–231 (2002).

    Article  Google Scholar 

  59. G. Lin, M. L. McCormack, C. Ma, and D. Guo, “Similar below-ground carbon cycling dynamics but contrsting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests,” New Phytol. 213, 1440–1451 (2017).

    Article  Google Scholar 

  60. B. D. Lindahl and A. Tunlid, “Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs,” New Phytol. 205, 1443–1447 (2015).

    Article  Google Scholar 

  61. R. W. Lucas and B. B. Casper, “Ectomycorrhizal community and extracellular enzyme activity following simulated atmospheric N deposition,” Soil Biol. Biochem. 40, 1662–1669 (2008).

    Article  Google Scholar 

  62. M. I. Makarov, V. G. Onipchenko, T. I. Malysheva, R. S. P. van Logtestijn, N. A. Soudzilovskaia, and J. H. C. Cornelissen, “Determinants of 15N natural abundance in leaves of co-occurring plant species and types within an alpine lichen heath in the Northern Caucasus,” Arct. Alp. Res. 46, 581–590 (2014).

    Article  Google Scholar 

  63. E. F. Malysheva, V. F. Malysheva, A. E. Kovalenko, E. A. Pimenova, M. N. Gromyko, S. N. Bondarchuk, and E. Yu. Voronina, “Below-ground ectomycorrhizal community structure in the post-fire successional Pinus koraiensis forests in the central Sikhote-Alin (the Russian Far East),” Bot. Pac. 5, 19–31 (2016).

    Google Scholar 

  64. J. Mayor, M. Bahram, T. Henkel, F. Buegger, K. Pritsch, and L. Tedersoo, “Ectomycorrhizal impacts on plant nitrogen nutrition: emerging isotopic patterns, latitudinal variation and hidden mechanisms,” Ecol. Lett. 18, 96–107 (2015).

    Article  Google Scholar 

  65. A. Michelsen, C. Quarmby, D. Sleep, and S. Jonasson, “Vascular plant 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots,” Oecologia 115, 406–418 (1998).

    Article  Google Scholar 

  66. A. Michelsen, I. K. Schmidt, S. Jonasson, C. Quarmby, and D. Sleep, “Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of nitrogen,” Oecologia 105, 53–63 (1996).

    Article  Google Scholar 

  67. Molecular Mycorrhizal Symbiosis, Ed. by F. Martin (Wiley, London, 2016).

    Google Scholar 

  68. K. Nadelhoffer, G. Shaver, B. Fry, A. Giblin, L. Johnson, and R. McKane, “15N natural abundances and N use by tundra plants,” Oecologia 107, 386–394 (1996).

  69. T. Näsholm, P. Högberg, O. Franklin, D. Metcalfe, S. G. Keel, C. Campbell, V. Hurry, S. Linder, and M. N. Högberg, “Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests?” New Phytol. 198, 214–221 (2013).

    Article  Google Scholar 

  70. E. E. Nuccio, A. Hodge, J. Pett-Ridge, D. J. Herman, P. K. Weber, and M. K. Firestone, “An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition,” Environ. Microbiol. 15, 1870–1881 (2013).

    Article  Google Scholar 

  71. M. Opik, M. Moora, J. Liira, and M. Zobel, “Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe,” J. Ecol. 94, 778–790 (2006).

    Article  Google Scholar 

  72. K. H. Orwin, M. U. F. Kirschbaum, M. G. St John, and I. A. Dickie, “Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment,” Ecol. Lett. 14, 493–502 (2011).

    Article  Google Scholar 

  73. L. H. Pardo, P. Semaoune, P. G. Schaberg, C. Eagar, and M. Sebilo, “Patterns in δ15N in roots, stems, and leaves of sugar maple and American beech seedlings, saplings and mature trees,” Biogeochemistry 112, 275–291 (2013).

    Article  Google Scholar 

  74. L. H. Pardo, P. H. Templer, C. L. Goodale, S. Duke, P. M. Groffman, M. B. Adams, P. Boeckx, J. Boggs, J. Campbell, B. Colman, J. Compton, B. Emmett, P. Gundersen, J. Kjonaas, G. Lovett, et al., “Regional assessment of N saturation using foliar and root delta N-15,” Biogeochemistry 80, 143–171 (2006).

    Article  Google Scholar 

  75. R. P. Phillips, E. Brzostec, and M. G. Midgley, “The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient coupling in temperate forests,” New Phytol. 199, 41–51 (2013).

    Article  Google Scholar 

  76. R. P. Phillips and T. J. Fahey, “Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings,” Global Change Biol. 11, 983–995 (2005).

    Article  Google Scholar 

  77. L. A. Phillips, V. Ward, and M. D. Jones, “Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests,” ISME J. 8, 699–713 (2014).

    Article  Google Scholar 

  78. D. J. Read, J. R. Leake, and J. Perez-Moreno, “Mycorrhizal fungi as drivers of ecosystem processes in heath land and boreal forest biomes,” Can. J. Bot. 82, 1243–1263 (2004).

    Article  Google Scholar 

  79. D. J. Read and J. Perez-Moreno, “Mycorrhizas and nutrient cycling in ecosystems: a journey towards relevance?” New Phytol. 157, 475–492 (2003).

    Article  Google Scholar 

  80. H. L. Reynolds, A. E. Hartley, K. M. Vogelsang, J. D. Bever, and P. A. Schultz, “Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture,” New Phytol. 167, 869–880 (2005).

    Article  Google Scholar 

  81. F. Rineau, D. Roth, F. Shah, M. Smits, T. Johansson, B. Canbäck, P. B. Olsen, P. Persson, M. N. Grell, E. Lindquist, I. V. Grigoriev, L. Lange, and A. Tunlid, “The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry,” Environ. Microbiol. 14, 1477–1487 (2012).

    Article  Google Scholar 

  82. F. Rineau, F. Shah, M. M. Smits, P. Persson, T. Johansson, R. Carleer, C. Troein, and A. Tunlid, “Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus,” ISME J. 7, 2010–2022 (2013).

    Article  Google Scholar 

  83. D. Robinson, L. L. Handley, and C. M. Scrimgeour, “A theory for 15N/14N fractionation in nitrate-grown vascular plants,” Planta 205, 397–406 (1998).

    Article  Google Scholar 

  84. D. Robinson, L. L. Handley, C. M. Scrimgeour, D. C. Gordon, B. P. Forster, and R. P. Ellis, “Using stable isotope natural abundances (δ15N and δ13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch) genotypes,” J. Exp. Bot. 51, 41–50 (2000).

    Google Scholar 

  85. D. Robinson, “δ15N as an integrator of the nitrogen cycle,” Trends Ecol. Evol. 16, 153–162 (2001).

    Article  Google Scholar 

  86. E.-D. Schulze, F.S. Chapin, III, and G. Gebauer, “Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska,” Oecologia 100, 406–412 (1994).

    Article  Google Scholar 

  87. P. F. Schweiger, “Nitrogen isotope fractionation during N uptake via arbuscular mycorrhizal and ectomycorrhizal fungi into grey alder,” J. Plant Physiol. 205, 84–92 (2016).

    Article  Google Scholar 

  88. O. Shtark, S. Kumari, R. Singh, A. Sulima, G. Akhtemova, V. Zhukov, A. Shcherbakov, E. Shcherbakova, A. Adholeya, and A. Borisov, “Advances and prospects for development of multi-component microbial inoculant for legumes,” Legume Persp. 8, 40–44 (2015).

    Google Scholar 

  89. S. E. Smith and D. J. Read, Mycorrhizal Symbiosis (Academic, London, 2008).

    Google Scholar 

  90. S. E. Smith and F. A. Smith, “Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales,” Annu. Rev. Plant Biol. 62, 227–250 (2011).

    Article  Google Scholar 

  91. J. M. Talbot, S. D. Allison, and K. K. Treseder, “Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change,” Funct. Ecol. 22, 955–963 (2008).

    Article  Google Scholar 

  92. J. M. Talbot and K. K. Treseder, “Controls over mycorrhizal uptake of organic nitrogen,” Pedobiologia 53, 169–179 (2010).

    Article  Google Scholar 

  93. L. Tedersoo, T. Naadel, M. Bahram, K. Pritsch, F. Buegger, M. Leal, U. Kõljalg, and K. Põldmaa, “Enzymatic activities and stable isotope patterns of ectomycorrhizal fungi in relation to phylogeny and exploration types in an Afrotropical rain forest,” New Phytol. 195, 832–843 (2012).

    Article  Google Scholar 

  94. C. Tian, B. Kasiborski, R. Koul, P. J. Lammers, H. Bucking, and Y. Shachar-Hill, “Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux,” Plant Physiol. 153, 1175–1187 (2010).

    Article  Google Scholar 

  95. S. D. Veresoglou, B. Chen, and M. C. Rillig, “Arbuscular mycorrhiza and soil nitrogen cycling,” Soil Biol. Biochem. 46, 53–62 (2012).

    Article  Google Scholar 

  96. S. D. Veresoglou, R. Sen, A. P. Mamolos, and D. S. Veresoglou, “Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils,” J. Ecol. 99, 1339–1349 (2011).

    Article  Google Scholar 

  97. J. F. Walker, L. Aldrich-Wolfe, A. Riffel, H. Barbare, N. B. Simpson, J. Trowbridge, and A. Jumpponen, “Diverse Helotiales associated with the roots of three species of Arctic Ericaceae provide no evidence for host specificity,” New Phytol. 191, 515–527 (2011).

    Article  Google Scholar 

  98. H. Wallander, H. Göransson, and U. Rosengren, “Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types,” Oecologia 139, 89–97 (2004).

    Article  Google Scholar 

  99. C. T. Wheeler, M. Tilak, C. M. Scrimgeour, J. E. Hooker, and L. L. Handley, “Effects of symbiosis with Frankia and arbuscular mycorrhizal fungus on the natural abundance of 15N in four species of Casuarina,” J. Exp. Bot. 51, 287–297 (2000).

    Article  Google Scholar 

  100. M. D. Whiteside, M. A. Digman, E. Gratton, and K. K. Treseder, “Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest,” Soil Biol. Biochem. 55, 7–13 (2012).

    Article  Google Scholar 

  101. M. D. Whiteside, K. K. Treseder, and P. R. Atsatt, “The brighter side of soils: quantum dots track organic nitrogen through fungi and plants,” Ecology 90, 100–108 (2009).

    Article  Google Scholar 

  102. N. Wurzburger and R. L. Hendrick, “Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest,” J. Ecol. 97, 528–536 (2009).

    Article  Google Scholar 

  103. N. Wurzburger and R. L. Hendrick, “Rhododendron thickets alter N cycling and soil extracellular enzyme activities in southern Appalachian hardwood forests,” Pedobiologia 50, 563–576 (2007).

    Article  Google Scholar 

  104. Y. Yano, G. R. Shaver, A. E. Giblin, and E. B. Rastetter, “Depleted N-15 in hydrolysable-N of arctic soils and its implication for mycorrhizal fungi–plant interaction,” Biogeochemistry 97, 183–194 (2010).

    Article  Google Scholar 

  105. T. Yoneyama and A. Kaneko, “Variations in the natural abundance of 15N in nitrogenous fractions in komatsuna plants supplied with nitrate,” Plant Cell Physiol. 30, 957–962 (1989).

    Google Scholar 

  106. T. Yoneyama, T. Omata, S. Nakata, and J. Yazaki, “Fractionation of nitrogen isotopes during the uptake and assimilation of ammonia by plants,” Plant Cell Physiol. 32, 1211–1217 (1991).

    Google Scholar 

  107. H. Yin, E. Wheeler, and R. P. Phillips, “Root-induced changes in nutrient cycling in forests depend on exudation rates,” Soil Biol. Biochem. 78, 213–221 (2014).

    Article  Google Scholar 

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ACKNOWLEDGMENTS

This study was supported by the Russian Science Foundation, project no. 16-14-10208

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  1. Lomonosov Moscow State University, Leninskie gory, 119991, Moscow, Russia

    M. I. Makarov

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Translated by D. Konyushkov

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Makarov, M.I. The Role of Mycorrhiza in Transformation of Nitrogen Compounds in Soil and Nitrogen Nutrition of Plants: A Review. Eurasian Soil Sc. 52, 193–205 (2019). https://doi.org/10.1134/S1064229319020108

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