• DOI: 10.31509/2658-607x-202471-141
  • УДК 574.472

ROLE OF WOODY PLANTS’ ECTOMYCORRHIZA IN THE DYNAMIC OF FOREST SOILS ORGANIC MATTER: SYNTHESIS AND CONCEPTUALIZATION OF AVAILABLE DATA

O. G. Chertov1*, I. V. Priputina2, V. N. Shanin1, 2, P. V. Frolov2

1 Center for Forest Ecology and Productivity of the Russian Academy of Sciences

Profsoyuznaya st., 84/32 bldg. 14, Moscow, 117997, Russian Federation

2Institute of Physical, Chemical and Biological Problems in Soil Science, Russian Academy of Sciences – separate subdivision of the Federal Research Centre

«Pushchino Research Centre of Russian Academy of Sciences»,

Russia, 142290, Moscow region, Pushchino, Institutskaya str., 2, build. 2.

*E-mail: ochertov@rambler.ru

Received: 20.02.2024

Revised: 15.03.2024

Accepted: 24.03.2024

The main aspects of the woody plants ectomycorrhiza functioning, which affect the forest soil organic matter (SOM) formation and decomposition, are considered. Ectomycorrhiza consumes trees’ root exudates for growth with formation of a dense net of extramatrical mycelium, which has a short life span. Thanks to that, a fast turnover of mycelium biomass takes place here with formation of a big pool of belowground litter fall. Its mass is larger than a total pool of aboveground litter (leaves, confer needles, etc.). Mycelial bio- and necromass have been consumed by soil biota of different functional groups and levels of soil food webs, resulting in formation of solid-phase metabolic products. These products (excreta, casts) represent a labile nitrogen-rich pool of fresh SOM. Simultaneously, the decomposition of this labile SOM pool serves as a mechanism to return available nitrogen to plant roots in the soil. This mechanism determines an ectomycorrhizal positive effect for trees and other plants growth in forest communities. Therefore, a consideration of the effect of ectomycorrhiza on soil organic matter shall include a triad of organisms: “plant – mycorrhiza – soil biota” (including both microorganisms and soil fauna).

Keywords: forest soils, ectomycorrhiza, soil organic matter, nitrogen mining, soil fauna, faunal excretes

 

REFERENCES

Aasfar A., Aasfar A., Bargaz A., Yaakoubi K., Hilali A., Bennis I., Zeroual Y., Meftah Kadmiri I., Nitrogen Fixing Azotobacter Species as Potential Soil Biological Enhancers for Crop Nutrition and Yield Stability, Frontiers in microbiology, 2021, Vol. 12, Article 628379.

Agerer R., Hartmann A., Pritsch K., Raidl S., Schloter M., Verma R., Weigt R., Plants and Their Ectomycorrhizosphere: Cost and Benefit of Symbiotic Soil Organisms, Growth and Defence in Plants. Resource Allocation at Multiple Scales, 2012, Vol. 220, рр. 213–242.

Akhmetzhanova A. A., Soudzilovskaia N. A., Onipchenko V. G., Cornwell W. K., Agafonov V. A., Selivanov I. A., Cornelissen J. H. C., A rediscovered treasure: Mycorrhizal intensity database for 3000 vascular plant species across the former Soviet Union, Ecology, 2012, Vol. 93, рр. 689–690.

Akkumuliatsiya ugleroda v lesnykh pochvakh i sukzessionnyi status lesov, (Carbon accumulation in forest soils and successional status of forests), N.V. Lukina (Ed.), Moscow, KMK, 2018, 232 p.

Albornoz F. E., Dixon K. W. Lambers H., Revisiting mycorrhizal dogmas: Are mycorrhizas really functioning as they are widely believed to do? Soil Ecology Letters, 2021, Vol. 3, рр. 73–82.

Arvieu J. C., Leprince F., Plassard C., Release of oxalate and protons by ectomycorrhizal fungi in response to P-deficiency and calcium carbonate in nutrient solution, Annals of Forest Science, 2003, Vol. 60, рр. 815–821.

Averill C., Bhatnagar J. M., Dietze M. C., Pearse W. D., Kivlin S. N., Global imprint of mycorrhizal fungi on whole-plant nutrient economics, PNAS, 2019, Vol. 116, No 46, рр. 23163–23168.

Bastida F., García C., Fierer N., Eldridge D. J., Bowker M. A., …, & Delgado-Baquerizo M., Global ecological predictors of the soil priming effect, Nature Communications, 2019, Vol. 10, рр. 3481.

Bazilevich N. I., Bioticheskiy krugovorot na piati kontinentakh: azot i zol’nyie elementy v prirodnykh nazemnykh ekosistemakh (Biotic turnover оn five continents: nitrogen and ash elements in natural terrestrial ecosystems), Novosibirsk, Siberian Branch Rus. Akad. Sciences, 2008, 376 p.

Becquer A., Guerrero C., Janice G., Eibensteiner L., Houdinet G., Bücking H., Zimmermann S. D., Garcia K., The ectomycorrhizal contribution to tree nutrition, Advances in Botanical Research, 2019, Vol. 89, рр. 77–126. 

Betekhtina А. А., Veselkin D. V., Mycorrhizal and non-mycorrhizal dicotyledonous herbaceous plants differ in root anatomy: evidence from the Middle Urals, Russia, Symbiosis, 2019, Vol. 77, No 2, рр. 133–140.

Björk R G., Ekblad A., Extramatrical mycelia production and turnover in two drained Norway spruce forests / I. Brunner (Ed.) Belowground carbon turnover in European forests – State of the art. COST Action FP0803 Conference, January 26–28, 2010, Swiss Federal Institute for Forest, Snow and Landscape Research WSL 2010, Birmensdorf, 2010, рр. 631–633.

Blagodatskaya Е., Kuzyakov   Y., Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review, Biology and Fertility of Soils, 2008, Vol. 45, рр. 115–131.

Blagodatsky S., Blagodatskaya E., Yuyukina T., Kuzyakov Y., Model of apparent and real priming effects: Linking microbial activity with soil organic matter decomposition, Soil biology and biochemistry, 2010, Vol. 42, рр. 1275–1283.

Bönisch E., Blagodatskaya E. Dirozo R., Ferlian O., Fichtner A., …, & Eisenhauer N., Mycorrhizal type and tree diversity affect foliar elemental pools and stoichiometry, The New Phytologist, 2024, PMID: 38594212, 15 p.

Brundrett M. C., Tedersoo L., Evolutionary history of mycorrhizal symbioses and global host plant diversity, The New Phytologist, 2008, Vol. 220, рр. 1108–1115.

Brundrett M. S., Diversity and classification of mycorrhizal associations, Biological reviews, 2004, Vol. 79, рр. 473–495.

Brunner I., Børja I., Dalsgaard L., Deckmyn G., Ekblad A., …, & Vanguelova E., Belowground carbon turnover of European forests: fine roots, mycorrhizal mycelia, soil organic matter and soil models. A Technical Report for National C reporters, LULUCF experts and ecosystem modellers, COST Action FP0803, Birmensdorf, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 2013, 67 p. 

Brzostek E. R., Fishe J. B., Phillip R. P., Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation, Journal of Geophysical Research: Biogeosciences, 2014, Vol. 119 (8), рр. 1684–1697.

Canarini A., Kaiser C., Merchant A., Richter A., Wanek W., Root exudation of primary metabolites: Mechanisms and their roles in plant responses to environmental stimuli, Frontiers in Plant Science, 2019, Vol. 10, рр. 157–165.

Chalot M., Brun A., Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas, FEMS Microbiology Reviews, 1998, Vol. 22, рр. 21–44.

Chertov O., Komarov A., Shaw C., Bykhovets S., Frolov P., …, & Shashkov M., Romul_Hum — A model of soil organic matter formation coupling with soil biota activity. II. Parameterisation of the soil food web biota activity, Ecological Modelling, 2017, Vol. 345, рр. 125–139.

Chertov O., Kuzyakov Y., Priputina I., Frolov P., Shanin V., Grabarnik P., Modelling the Rhizosphere Priming Effect in Combination with Soil Food Webs to Quantify Interaction between Living Plant, Soil Biota and Soil Organic Matter, Plants, 2022, Vol. 11, Article 2605.

Choreno-Parra E. M., Treseder K. K., Mycorrhizal fungi modify decomposition: a meta analysis, The New Phytologist, 2024, Vol. 242, No 6, рр. 2763–2774.

de Vries F. T., Caruso T., Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web, Soil biology and biochemistry, 2016, Vol. 102, рр. 4–9.

de Vries F. T., Thébault E., Liiri M., Birkhofer K., Tsiafouli M. A., et al., Soil food web properties explain ecosystem services across European land use systems, Proceedings of the National Academy of Sciences, 2013, Vol. 110, рр. 14296–14301.

Deckmyn G., Meyer A., Smits M.M., Ekblad A., Greben T., Komarov A., Kraigher H., Simulating ectomycorrhizal fungi and their role in carbon and nitrogen cycling in forest ecosystems, Canadian Journal of Forest Research, 2014, Vol. 44, No 6, рр. 535–553.

Dudka V. A., Malysheva E. F., Malysheva V. F., Zhukova E. A. Mikoriza lipy (Tilia spp.) v iskusstvennykh nasazhdeniyakh Sankt Peterburga (Lime (Tilia spp.) mycorrhiza at artificial planting of St.Petersburg), Mikologia i Phytopatalogiya, 2021, Vol. 55, No 1, pp. 11–35.

Ekblad A., Wallander H., Godbold D. L., Cruz C., Johnson D., …, & Plassard C., The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling of extramatrical mycelium (EMM) of mycorrhizal fungi in carbon (C) cycling in ecosystems, Plant Soil, 2013, Vol. 366, рр. 1–27.

Fogel R., Hunt G., Contribution of mycorrhizal and soil fungi to nutrient cycling in a Douglas-fir ecosystem, Canadian Journal of Forest Research, 1983, Vol. 13 (2), рр. 219–232.

Gadd G. M., Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation, Mycological research, 2007, Vol 111, рр. 3–49, DOI: 10.1016/j.mycres.2006.12.001.

Geisen S., Koller R., Hünninghaus M., Dumack K., Urich T., Bonkowski M., The soil food web revisited: Diverse and widespread mycophagous soil protists, Soil biology and biochemistry, 2016, Vol. 94, рр. 10–18, DOI: 10.1016/j.soilbio.2015.11.010.

Godbold D. L., Hoosbeek M. R., Lukac M., Cotrufo M. F., Janssens I. A., …, & Prescott A., Mycorrhizal hyphal turnover as a dominant process for C input into soil organic matter, Plant Soil, 2006, Vol. 281, рр.15–24.

Gorka S., Dietrich M., Mayerhofer W., Gabriel R., Wiesenbauer J., …, & Kaiser C., Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability, Frontiers in microbiology, 2019, Vol. 10, Article 168, DOI: 10.3389/fmicb.2019.00168.

Guignabert A., Delerue F., Gonzalez M., Augusto L., Bakker M., Effects of Management Practices and Topography on Ectomycorrhizal Fungi of Maritime Pine during Seedling Recruitment, Forests, 2018, Vol. 9, No 5, DOI: 10.3390/f9050245.

Hanajima D., Aoyagi T., Hori T., Dead bacterial biomass-assimilating bacterial populations in compost revealed by high-sensitivity stable isotope probing, Environment International, 2019, Vol. 133, Article 105235, DOI: 10.1016/j.envint.2019.

Hawkins H.-J., Cargill R. I. M., Van Nuland M. E., Hagen S. C., Field K. J., Sheldrake M., Soudzilovskaia N., Kiers E. T., Review. Mycorrhizal mycelium as a global carbon pool, Current Biology, 2023, Vol. 33, No 11,  Article R560–R573.

He Y. H., Cheng W. X., Zhou L. Y., Shao J. J., Liu H. Y., Zhou H. M., Zhu K., Zhou X. H., Soil DOC release and aggregate disruption mediate rhizosphere priming effect on soil C decomposition, Soil biology and biochemistry, 2020, Vol. 144, Article 107787, DOI: 10.1016/j.soilbio.2020.107787.

Hobbie E. A., Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies, Ecology, 2006, Vol. 87, рр. 563–569, DOI: 10.1890/05-0755.

Hobbie E. A., Ouimette A. P., Schuur E. A. G., Kierstead D., Trappe J. M., Bendiksen K., Ohenoja E., Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi, Biogeochemistry, 2013, Vol. 114, рр. 381–389, DOI: 10.1007/s10533-012-9779-z.

Hoffrichter R., Griby. Obitateli skrytogo mira (Fungi. Inhaitants of the hidden world), Moscow, Azbuka, 2021, 280 p.

Högberg M. N., Högberg P., Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil, The New Phytologist, 2002, Vol. 154, рр. 791–795, DOI: 10.1046/j.1469-8137.2002.00417.x.

Holtkamp R., van der Wal A., Kardol P., van der Putten W. H., de Ruiter P. C., Dekker S. C., Modelling C and N mineralisation in sol food webs during secondary succession on ex-arable land, Soil biology and biochemistry, 2011, Vol. 43, рр. 251–260.

Huang Ye, Guenet B., Ciais P., Janssens I.A., Soong J. L., Wang Y., Goll D., Blagodatskaya E., Huang Yu., ORCHIMIC (v1.0), A microbe-mediated model for soil organic matter decomposition, Geoscientific Model Development, 2018, Vol. 11, рр. 2111–2138, DOI: 10.5194/gmd-11-2111-2018. 

Iozus A. P., Zavialov A. A. Boiko S. Yu., Osobennosty vliyaniya mikorizy na prizhivaemost’ I biokhimicheskiy sostsv seyantsev sosny obyknovennoy v sukhoy syepi Nizhnego Povolzhiya (Special patterns of mycorrhiza’s influence on Scots pine seedlings survival in dry steppe of Lower Volga Valley), Uspekhi sovremennogo estestvoznanniya, 2019, No 6, pp. 23–27.

Jacquemyn H., Merckx V. S. F. T., Mycorrhizal symbioses and the evolution of trophic modes in plants, Journal of Ecology, 2019, Vol. 107, рр. 1567–1581, DOI: 10.1111/1365-2745.13165.

Jentschke G., Bonkowski M., Godbold D. L., Scheu S., Soil protozoa and forest tree growth: non-nutritional effects and interaction with mycorrhizae, AGRIS, 2013, Vol. 20, рр. 263–269, DOI: 10.1007/BF00336088.

Johansson E. M., Fransson P. M. A., Finlay R. D., van Hees P. A. W., Quantitative analysis of root and ectomycorrhizal exudates as a response to Pb, Cd and as stress, Plant Soil, 2008, Vol. 313, рр. 39–54, DOI: 10.1007/s11104-008-967. 

Johnson N. C., Graham J. H., The continuum concept remains a useful framework for studying mycorrhizal functioning, Plant Soil, 2013, Vol. 363, рр. 411−419, DOI: 10.1007/s11104-012-1406.

Johnson N. C., Wilson G. W. T., Wilson J. A., Miller R. M., Bowker M. A., Mycorrhizal phenotypes and the law of the minimum, The New Phytologist, 2015, Vol. 205, рр. 1473–1484. DOI: 10.1111/nph.13172.

Jones D. L., Hodge A., Kuzyakov Y., Plant and mycorrhizal regulation of rhizodeposition, The New Phytologist, 2004, Vol. 163, рр. 459–480, DOI: 10.1111/j.1469-8137.2004.01130.x.

Kaiser C., Merchant A., Richter A., Wanek W., Root exudation of primary metabolites: Mechanisms and their roles in plant responses to environmental stimuli, Frontiers in Plant Science, 2019, Vol. 10, Article 157, DOI: 10.3389/fpls.2019.00157. 

Kalinina O., Cherkinsky A., Chertov O., Goryachkin S., Kurganova I., Lopes de Gerenyu V., Lyuri D., Kuzyakov Y., Giani L., Post-agricultural restoration: Implications for dynamics of soil organic matter pools, Catena, 2019, Vol. 181, Article 104096, DOI: 10.1016/j.catena.2019.104096.

Klink S., Keller A. B., Wildae A. J., Baumert V. L., Gube M., …, & Pausch J., Stable isotopes reveal that fungal residues contribute more to mineral-associated organic matter pools than plant residues, Soil biology and biochemistry, 2022, Vol. 168, Article 108634, DOI: 10.1016/j.soilbio.2024.109323.

Kolmakov P. Yu., Kisova A. S., Raznoobrazie ektomikoriz Picea abies v estestvennykh mestoobitaniyakh Belorusskogo Poozerya (Diversity of Picea abies ectomycorrhizas in natural conditions of Belorussian Lake Region), Materialy II Mezhdunarodnoy konferentsii, 20-23 sentiabria 2016 “biologiya. Sistematika I ekologiya gribov i lishaynikov v prirodnykh ekosistemakh i agrofitotsenozakh, 2016, Minsk, pp. 123–125.

Komarov A., Chertov O., Bykhovets S., Shaw C., Nadporozhskaya M., … & Zubkova E., Romul_Hum model of soil organic matter formation coupled with soil biota activity. I. Problem formulation, model description, and testing, Ecological Modelling, 2017, Vol. 345, рр. 113–124, DOI: 10.1016/j.ecolmodel.2016.08.007.

Kranabetter J. M., Ectomycorrhizal fungi and the nitrogen economy of conifers—implications for genecology and climate change mitigation, Botany, 2014, Vol. 92, рр. 417–423, DOI: 10.1139/cjb-2013-0198.

Kuzyakov Y., Hill P. W., Jones D. L., Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature, Plant Soil, 2007, Vol. 290, рр. 293–305.

Lavrenov N. G., Zernov A. S., Kipreev A. M., et al. Mikoriza rastenyi v ekstremalnykh usloviyakh: alpiyskiye kovry Armenii (Plants’ mycorrhiza in extremal conditions: alpen covers of Armenia), Zhurnal obshchey biologii, 2017, Vo. 78, No 4, pp. 80–85.

Lei X., Shen Y., Zhao J., Huang J., Wang H., Yu Y., Xiao C., Review: root exudates mediate the processes of soil organic carboni and efflux, Plants, 2023, Vol. 12 (3), Article 630, DOI: 10.3390/plants12030630.

Liese R., Lübbe T., Albers N. W., Meier I. C., The mycorrhizal type governs root exudation and nitrogen uptake of temperate tree species, Tree Physiology, 2018, Vol. 38, рр. 83–95,  DOI: 10.1093/treephys/tpx131.

Lindahl B. D., Tunlid A., Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs, The New Phytologist, 2015, Vol. 205, No 4, рр. 1443–1447.

Lukac M., Calfapietra C., Godbold D. L., Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE), Global Change Biology, 2003, Vol. 9, рр. 838–848, DOI: 10.1046/j.1365-2486.2003.00582.x.

Lukina N. V., Chibrik T. S., Glazyrina M. A., Filimonova E. I., Dinamika vosstanovleniya rastitelnosti Iimikorizy na rekultivirovannakh i nerekultivirovannykh uchstkah zolootvala Verkhnitagilskoy GRES (Srednyi Ural) (Dynamics of vegetation and mycorrhiza restoration on restored and non-restored sites on ash dump of Verkhnitagilsk power plant (Middle Ural). Ekosistemy, 2019, No 20 (50), pp. 188–196.

Makarov M. I., Rol’ mikorizy v transformatsii soedineny azota v pochve I v azotnom pitanii rasteniy (obzor) (Role of mycorrhiza nitrogen compounds transformation and in plants’ nitrogen nutrition (review), Pochvovedeine (Eurasian Soil Science), 2019, No 2, pp. 220–233.

Manzoni S., Porporat A., Soil carbon and nitrogen mineralization: theory and models across scales, Soil biology and biochemistry, 2009, Vol. 41, рр. 1355–1379, DOI: 10.1016/j.soilbio.2009.02.031.

Martin F., (Ed.) Molecular Mycorrhizal Symbiosis, John Wiley & Sons, Hoboken, New Jersey, 2017, 506 p.

Martin F., Kohler, A., Murat C., Veneault-Fourrey C., Hibbett D. S., Unearthing the roots of ectomycorrhizal symbioses, Nature Reviews Microbiology, 2016, Vol. 14 (12), рр. 760–773. DOI: 10.1038/nrmicro.2016.149

Meyer A., Grote R., Butterbach-Bahl K., Integrating mycorrhiza in a complex model system: effects on ecosystem C and N fluxes, European journal of forest research, 2012, Vol. 131 (6), рр. 1809–1831, DOI: 10.1007/s10342-012-0634-5.

Meyer A., Grote R., Pol A., Simulating mycorrhiza contribution to forest C- and N cycling – the MYCOFON model, Plant Soil, 2010, Vol. 327, рр. 493–517, DOI: 10.1007/s11104-009-0017-y.

Mus F., Crook M. B., Garcia K., Garcia Costas A., Geddes B. A., …, & Peters J. W., Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes, Applied and environmental microbiology, 2016, Vol. 82, рр. 3698 –3710, DOI: 10.1128/AEM.01055-16.

Nehls U., Das A., Neb D., Carbohydrate metabolism in ectomycorrhizal symbiosis [in:] F. Martin (Ed.) Molecular Mycorrhizal Symbiosis, Chapter 10, John Wiley & Sons, 2017, рр. 161–177.

Nehls U., Göhringer F., Wittulsky S., Dietz S., Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review, Plant Biology, 2010, Vol. 12 (2), рр. 292–301, DOI: 10.1111/j.1438-8677.2009.00312.x.

O’Hanlon R., Below-ground ectomycorrhizal communities: the effect of small scale spatial and short term temporal variation, Symbiosis, 2012, Vol. 57, рр. 57–71, DOI: 10.1007/s13199-012-0179.  

Odum E., Ekologiya (Ecology). Moscow, Mir. 1986. Vol. 1, 328 p., Vol. 2, 376 p.

Pang W., Zhang P., Zhang Y., Zhang X., Huang Y., Zhang T., Liu B., The ectomycorrhizal fungi and soil bacterial communities of the five typical tree species in the Junzifeng National Nature Reserve, Southeast China, Plants, 2023, Vol. 12, Article 3853, DOI: 10.3390/plants12223853.

Pausch J., Kramer S., Scharroba A., Scheunemann N., Butenschoen O., …, & Ruess L., Small but active – pool size does not matter for carbon incorporation in belowground food webs, Functional Ecology, 2016, Vol. 30, рр. 479–489, DOI: 10.1111/1365-2435.12512.

Pausch J., Tian, J., Riederer M., Kuzyakov Y., Estimation of rhizodeposition at field scale: Upscaling of a 14C labeling study, Plant Soil, 2013, Vol. 364, рр. 273–285, DOI: 10.1007/s11104-012-1363-8.83.

Pena R., Nitrogen aquisition in ectomicorrhizal symbiosis [in:] Martin F. (Ed.) Molecular Mycorrhizal Symbiosis, Chapter 11, John Wiley & Sons, 2017, рр. 178–196.

Ponomareva V. V., Teoriya podzoloobrazovatelnogo protsessa. Biokhimicheskie aspekty (Theory of podzol formation process, Biochemical aspects), Moscow, Nauka, 1964, 379 p.

Rineau F., Shah F., Smits M.M., Persson P., Johansson T., Carleer R., Troein C., Tunlid A., Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus, The ISME journal, 2013, Vol. 7 (10), рр. 2010–2022, DOI: 10.1038/ismej.2013.91.

Saifuddin M., Bhatnagar J. M., Phillips R. P., Finzi A. C., Ectomycorrhizal fungi are associated with reduced nitrogen cycling rates in temperate forest soils without corresponding trends in bacterial functional groups, Oecologia, 2021, Vol. 196, рр. 863–875.

Savolainen T., Kytöviita M.-M., Mycorrhizal symbiosis changes host nitrogen source use, Plant Soil, 2022, Vol. 471, рр. 643–654.

Schröter D., Wolters V., De Ruiter P., C and N mineralisation in the decomposer food webs of a European forest transect, Oikos, 2003, Vol. 102, рр. 294–308, DOI: 10.1034/j.1600-0579.2003.12064.x.

Sergeeva M. N., Griby. Bolshaya enciklopedia (Fungi/Mushrooms. Big encyclopedia), Moscow, Ast, 2022, 256 p.

Simard S. W., Beiler K. J., Bingham M. A., Deslippe J. R., Philip L. J., Teste F. P., Mycorrhizal networks: mechanisms, ecology and modelling, Fungal Biology Reviews, 2012, Vol. 26, рр. 39–60, DOI: 10.1016/j.fbr.2012.01.001.

Smith S. E., Read D. J. Mycorrhizal symbiosis. 3rd ed. Academic Press, Amsterdam, 2008. DOI: 10.1016/B978-0-12-370526-6.X5001-6.

Smith S. E., Read D. J., MikoriznyK simbioz (Mycorrhizal symbiosis), Moscow, KMK, 2012, 776 p.

Smits M., Wallander H. Role of Mycorrhizal Symbiosis in Mineral Weathering and Nutrient Mining from Soil Parent Material. Chapter 3 [in:] N. C. Johnson, C. Gehring, J. Jansa (Eds.) Mycorrhizal Mediation of Soil. Elsevier, 2017. P. 35–46. DOI: 10.1016/B978-0-12-804312-7.00003-6.

Soudzilovskaia N. A., Vaessen S., van’t Zelfde M., Raes N., Global patterns of mycorrhizal distribution and their environmental drivers [in:] L. Tedersoo (Ed.) Biogeography of Mycorrhizal Symbiosis. Ecological Studies, Vol. 230, Springer, 2017, рр. 223–235, DOI: 10.1007/978-3-319-56363-3_11.

Staddon P. L., Mycorrhizal fungi and environmental change: the need for a mycocentric approach // The New Phytologist. 2005. Vol. 167. P. 635–637.

Staddon P. L., Ramsey C. B., Ostle N., Ineson P., Fitter A. H. Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C, Science, 2003, Vol. 300, рр. 1138–1140, DOI: 10.1126/science.1084269.

Stuart E. K., Plett K. L., Digging deeper: in search of the mechanisms of carbon and nitrogen exchange in ectomycorrhizal symbioses, Frontiers in Plant Science, 2020, Vol. 10. Article 1658,  DOI: 10.3389/fpls.2019.01658.

Sun L., Ataka M., Han M., Han Y., Gan D., Xu T., Guo Y., Zhu B., Root exudation as a major competitive fine-root functional trait of 18 coexisting species in a subtropical forest, The New Phytologist, 2020, Vol. 229 (1), рр. 259–271, DOI: 10.1111/nph.16865.

Sun Q., Fu Z., Finlay R., Lian B., Transcriptome analysis provides novel insights into the capacity of the ectomycorrhizal fungus Amanita pantherina to weather K-containing feldspar and apatite, Applied and Environmental Microbiology, 2019, Vol. 85 (15), Article e00719-19.

Talbot J. M., Allison S. D., Treseder K. K., Decomposers in disguise: Mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change, Functional ecology, 2008, Vol. 22, рр. 955–963, DOI: 10.1111/j.1365-2435.2008.01402.x.

Talbot J. M., Bruns T. D., Smith D. P., Branco S., Glassman S. I., Erlandson S., Vilgalys R., Peay K. G., Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition, Soil biology and biochemistry, 2013, Vol. 57, рр. 282–291, DOI: 10.1016/j.soilbio.2012.10.004.

Tedersoo L., (Ed.) Biogeography of mycorrhizal symbiosis, Vol. 230, Springer, 2017, 566 p. DOI: 10.1007/978-3-319-56363-3.

Tedersoo L., Bahram M., Zobel M., How mycorrhizal associations drive plant population and community biology, Science, 2020, Vol. 367 (6480), Article eaba1223, DOI: 10.1126/science.aba1223.

Threatt S. D., Rees D. C., Biological Nitrogen Fixation. In Theory, Practice, and Reality: A Perspective on the Molybdenum Nitrogenase System, FEBS Letters, 2023, Vol. 597 (1), рр. 45–58,  DOI: 10.1002/1873-3468.14534.

Titlianova A. A., Sambuu A. D., Sukzessii v travianykh ekosistemakh (Successions in grassland ecosystems), Novosibirsk, Siberian Branch Rus. Acad. Sci., 191 p.

Tiunov A. V., Troficheskie seti v pochve borealnogo lesa: v poiskakh znacheniya mikorizy (food webs in soil of boreal forest: searching mycorrhiza’s importance), v kn. Problemy pochvennoy zoologii. Materialy XVII Vserossiskogo soveschaniya po pochvennoy zoologii, posviashchennogo 75-letiyu chlen-korrespondenta RAN D. A. Krivolutskogo, 2014, pp. 220–222.

Tunlid A., Floudas D., Koide R., Rineau F., Soil organic matter decomposition mechanisms in ectomycorrhizal fungi, Molecular, Mycorrhizal Symbiosis, 2017, DOI: 10.1002/9781118951446. P. 257–275. DOI: 10.1002/9781118951446.

van Breemen N., Finlay R., Lundström U., Jongmans A. G., Giesler R., Olsson M., Mycorrhizal weathering: A true case of mineral plant nutrition?  Biogeochemistry, 2000, Vol. 49, рр. 53–67, DOI: 10.1023/A:1006256231670.

Van der Heijden M. G. A., Horton T. R., Socialism in Soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems, Journal of ecology, 2009, Vol. 97, рр. 1139–1150. DOI: 10.1111/j.1365-2745.2009.01570.x.

Van Hees P. A. W., Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris, The New Phytologist, 2005, Vol. 169 (2), рр. 367–378, DOI: 10.1111/j.1469-8137.2005.01600.x.

Veselkin D. V. Sootnosheniye ob’emov griba i drevesnykh tkaney v ektomikoriznykh korniakh khvoinykh (Proportion of volumes between mycelium and wood tissues in ectomycorrhiza roots of coniferous), Ledovedenie, 2015, No 2, pp. 140–146.

Veselkin D. V., Lukina N. V., Chibrik T. S., Sootnosheniye mikoriznykh i nemikoriznykh vidov rasteniy v pervichnykh tekhnogennykh sukzessiyakh (Proportion of mycorrhiza and non-mycorrhiza plant species at primary technogenic succession), Ekologiya, 2015, No 5, pp.  345–352.

Veselkin D. V., Morfologicheskaya izmenchivost i adaptivnoe znachenie ektomikoriz khvoinykh (Pinaceae Lindl.) (Morphological variability and adaptive significance of coniferous mycorrhiza (Pinaceae Lindl.), Avtoref, diss. dokt. biol. nauk, 2013, 40 p.

Volobueva O. G., Simbioticheskaya azotfiksatsiya kak factor ekologicheskoy bezopasnosty i plodorodiya pochvy (Symbiotiv nitrogen fixation as a factor of ecological security and soil fertility). Veatnik of Rostov Uni. Frendship of Peoples, Ecology and life security iss., 2011, No 1, pp. 53–60.

Voronina E. Yu. Mikorizy i ikn rol’ v formirovanii communities (Mycorrhizaz and their role in (plant) communities’ formation), Vestnik Moskovskogo universiteta, Seria 16 Biologiya, 2006, No 4, pp. 17–27.

Voronina E. Yu., Mikorizy v nazemnykh ekosistemakh: ekologicheskie, fizziologicheskie i molekuliarno-geneticheskie aspect mikoriznykh simbiozov (Micorrhizas in terrestrial ecosystems: ecological, physiological and molecular-genetic aspects of mycorrhizal symbioses), v kn.: Mikologiya segodnia (Mycology today). Ju. T. Dyakov, A. Ju Sergeev (Eds.). Natsionalnaya Akademiea Mikologii, Moscow, 2007, pp. 101–192.

Wallander H., Nilsson L. O., Hagerberg D., Bååth E., Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field, The New Phytologist, 2001, Vol. 151, рр. 753–760, DOI: 10.1046/j.0028-646x.2001.00199.x.

Wang B., An S., Liang C., Liu Y., Kuzyakov Y., Microbial necromass as the source of soil organic carbon in global ecosystems, Soil Biology and Biochemistry, 2021, Vol. 162, Article 108422,  DOI: 10.1016/j.soilbio.2021.108422.

Wang Q., Xing Y., Luo Xi, Liu G., Yan G., Changes in ectomycorrhizal and saprophytic fungal communities during a secondary succession of temperate forests, European Journal of Forest Research, 2023, Vol. 142, рр. 1313–1323.

Wauke R., Ispolzovanie mikorizy v sadodvodstve kak metod resheniya problem v oblastti ekologicheskogo vozdelyvaniya rastenyi (Use of mycorrhiza in orchards agriculture as a method of problems solution at ecological agriculture), Plodovodstvo i yagogovodstvo Rossii, 2005, Vol, 14, pp. 234–244.

Zhou J., Zang H., Loeppmann S., Gube M., Kuzyakov Y., Pausch J., Arbuscular mycorrhiza enhances rhizodeposition and reduces the rhizosphere priming effect on the decomposition of soil organic matter, Soil biology and biochemistry, 2020, Vol. 140, Article 107641, DOI: 10.1016/j.soilbio.2019.107641.