Skip to main content

Arbuscular Mycorrhiza in Sustainable Plant Nitrogen Nutrition: Mechanisms and Impact

  • Chapter
  • First Online:
Book cover Soil Nitrogen Ecology

Abstract

Nitrogen (N) is an important macronutrient that has a significant role in plant growth and development. Therefore, optimum levels of N should be supplied to the plants for sustainable crop production. Besides the chemical fertilization of plants, beneficial soil microorganisms like the arbuscular mycorrhizal (AM) fungi form a mutualistic association with the majority of plant roots and enhance plant growth and nutrient uptake. The importance of AM fungi is mostly attributed to phosphorus (P) acquisition in plants. Nevertheless, the role of AM fungi in the N nutrition of plants is also well known. Plants N acquisition is mediated by direct and indirect pathways through plant roots or via a common mycelium network of AM fungi. Organic and inorganic N is the major source of N in the soils. Influence of AM fungi on other symbiotic and asymbiotic microorganisms is also known to contribute to dinitrogen (N2) fixation in plants. This chapter highlights the role of AM fungi in N nutrition, N2 fixation, and uptake of organic and inorganic N from the soils. Also, the importance of AM fungi in the N cycle and the impact of different AM fungal species on plant N uptake are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Almonacid L, Fuentes A, Ortiz J, Salas C, Garcia-Romera I, Ocampo J, Arriagada C (2015) Effect of mixing soil saprophytic fungi with organic residues on the response of Solanum lycopersicum to arbuscular mycorrhizal fungi. Soil Use Manag 31:155–164

    Article  Google Scholar 

  • An H, Owens J, Stoeckli J, Hao X, Beres B, Li Y (2020) Nitrous oxide emissions following split fertilizer application on winter wheat grown on Mollisols of southern Alberta, Canada. Geoderma Reg 21:e00272. https://doi.org/10.1016/j.geodrs.2020.e00272

    Article  Google Scholar 

  • Arriagada C, Almonacid L, Cornejo P, Garcia-Romera I, Ocampo J (2014) Influence of an organic amendment comprising saprophytic and mycorrhizal fungi on soil quality and growth of Eucalyptus globulus in the presence of sewage sludge contaminated with aluminium. Arch Agron Soil Sci 60:1229–1248

    Article  CAS  Google Scholar 

  • Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246

    Article  CAS  PubMed  Google Scholar 

  • Avrahami S, Bohannan BJ (2007) Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. App Environ Microbiol 73:1166–1173

    Article  CAS  Google Scholar 

  • Bahadur A, Jin Z, Long X, Jiang S, Zhang Q, Pan J, Liu Y, Feng H (2019) Arbuscular mycorrhizal fungi alter plant interspecific interaction under nitrogen fertilization. Eur J Soil Biol 93:103094. https://doi.org/10.1016/j.ejsobi.2019.103094

    Article  Google Scholar 

  • Bai B, Suri VK, Kumar A, Choudhary AK (2016) Influence of dual inoculation of AM fungi and Rhizobium on growth indices, production economics, and nutrient use efficiencies in garden pea (Pisum sativum L.). Commun Soil Sci Plant Anal 47:941–954

    Article  CAS  Google Scholar 

  • Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  CAS  PubMed  Google Scholar 

  • Barrow CJ (2012) Biochar potential for countering land degradation and for improving agriculture. Appl Geogr 34:21–28

    Article  Google Scholar 

  • Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45

    Article  Google Scholar 

  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ahmed N, Ashraf M, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068

    Article  PubMed  PubMed Central  Google Scholar 

  • Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11

    Article  CAS  Google Scholar 

  • Bowles TM, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Environ 566:1223–1234

    Article  PubMed  CAS  Google Scholar 

  • Bowles TM, Jackson LE, Cavagnaro TR (2018) Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob Chang Biol 24:e171–e182. https://doi.org/10.1111/gcb.13884

    Article  PubMed  Google Scholar 

  • Breuninger M, Trujillo CG, Serrano E, Fischer R, Requena N (2004) Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet Biol 41:542–552

    Article  CAS  PubMed  Google Scholar 

  • Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    Article  CAS  Google Scholar 

  • Bücking H, Kafle A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587–612

    Article  CAS  Google Scholar 

  • Bücking H, Mensah JA, Fellbaum CR (2016) Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. Commun Integr Biol 9:e1107684. https://doi.org/10.1080/19420889.2015.1107684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukovská P, Gryndler M, Gryndlerová H, Püschel D, Jansa J (2016) Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. Front Microbiol 7:711. https://doi.org/10.3389/fmicb.2016.00711

    Article  PubMed  PubMed Central  Google Scholar 

  • Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, Řezáčová V, Gutiérrez-Núñez MS, Gryndler M, Jansa J (2018) Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers? Mycorrhiza 28:269–283

    Article  PubMed  CAS  Google Scholar 

  • Bulgarelli RG, Marcos FC, Ribeiro RV, de Andrade SA (2017) Mycorrhizae enhance nitrogen fixation and photosynthesis in phosphorus-starved soybean (Glycine max L. Merrill). Environ Exp Bot 140:26–33

    Article  CAS  Google Scholar 

  • Cappellazzo G, Lanfranco L, Bonfante P (2007) A limiting source of organic nitrogen induces specific transcriptional responses in the extraradical structures of the endomycorrhizal fungus Glomus intraradices. Curr Genet 51:59. https://doi.org/10.1007/s00294-006-0101-2

    Article  CAS  PubMed  Google Scholar 

  • Cavagnaro TR, Barrios-Masias FH, Jackson LE (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant Soil 353:181–194

    Article  CAS  Google Scholar 

  • Cely MV, De Oliveira AG, De Freitas VF, de Luca MB, Barazetti AR, Dos Santos IM, Gionco B, Garcia GV, Prete CE, Andrade G (2016) Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Front Microbiol 7:720. https://doi.org/10.3389/fmicb.2016.00720

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapagain T, Riseman A (2014) Barley–pea intercropping: effects on land productivity, carbon and nitrogen transformations. Field Crops Res 166:18–25

    Article  Google Scholar 

  • Chen H, Hicks W (2003) High asymbiotic N2 fixation rates in woody roots after six years of decomposition: controls and implications. Basic Appl Ecol 4:479–486

    Article  Google Scholar 

  • Chen Y, Yu Z, Wang J, Zhang X (2014) Allocation of photosynthetic carbon to nodules of soybean in three geographically different Mollisols. Euro J Soil Biol 62:60–65

    Article  CAS  Google Scholar 

  • Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Jiang Y, Liu A, Zhao P, Wang M, Ahammed GJ (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:2516. https://doi.org/10.3389/fmicb.2017.02516

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi–from ecology to application. Front Plant Sci 9:1270. https://doi.org/10.3389/fpls.2018.01270

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  CAS  PubMed  Google Scholar 

  • Christou M, Avramides EJ, Jones DL (2006) Dissolved organic nitrogen dynamics in a Mediterranean vineyard soil. Soil Biol Biochem 38:2265–2277

    Article  CAS  Google Scholar 

  • Coelho MR, Marriel IE, Jenkins SN, Lanyon CV, Seldin L, O’Donnell AG (2009) Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer. Appl Soil Ecol 42:48–53

    Article  Google Scholar 

  • Cormier F, Foulkes J, Hirel B, Gouache D, Moënne-Loccoz Y, Le Gouis J (2016) Breeding for increased nitrogen-use efficiency: a review for wheat (T. aestivum L.). Plant Breed 135:255–278

    Article  CAS  Google Scholar 

  • Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dal Cortivo C, Ferrari M, Visioli G, Lauro M, Fornasier F, Barion G, Panozzo A, Vamerali T (2020) Effects of seed-applied biofertilizers on rhizosphere biodiversity and growth of common wheat (Triticum aestivum L.) in the field. Front Plant Sci 11:72. https://doi.org/10.3389/fpls.2020.00072

    Article  PubMed  PubMed Central  Google Scholar 

  • de Novais CB, Sbrana C, da Conceição Jesus E, Rouws LF, Giovannetti M, Avio L, Siqueira JO, Júnior OJ, da Silva EM, de Faria SM (2020) Mycorrhizal networks facilitate the colonization of legume roots by a symbiotic nitrogen-fixing bacterium. Mycorrhiza 25:1–8

    Google Scholar 

  • Diagne N, Baudoin E, Svistoonoff S, Ouattara C, Diouf D, Kane A, Ndiaye C, Noba K, Bogusz D Franche C, Duponnois R (2018) Effect of native and allochthonous arbuscular mycorrhizal fungi on Casuarina equisetifolia growth and its root bacterial community. Arid Land Res Manag 32:212–228

    Article  Google Scholar 

  • Dion PP, Jämtgård S, Bertrand A, Pepin S, Dorais M (2018) Organic nitrogen uptake and assimilation in Cucumis sativus using position-specific labeling and compound-specific isotope analysis. Front Plant Sci 9:1596. https://doi.org/10.3389/fpls.2018.01596

    Article  PubMed  PubMed Central  Google Scholar 

  • Dutta SC, Neog B (2017) Inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria in modulating phosphorus dynamics in turmeric rhizosphere. Natl Acad Sci Lett 40:445–449

    Article  CAS  Google Scholar 

  • Ercoli L, Schüßler A, Arduini I, Pellegrino E (2017) Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities. Plant Soil 419:153–167

    Article  CAS  Google Scholar 

  • Fan F, Yang Q, Li Z, Wei D, Cui XA, Liang Y (2011) Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb Ecol 62:982–990

    Article  PubMed  Google Scholar 

  • Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012a) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fellbaum CR, Mensah JA, Pfeffer PE, Kiers ET, Bücking H (2012b) The role of carbon in fungal nutrient uptake and transport: implications for resource exchange in the arbuscular mycorrhizal symbiosis. Plant Signal Behav 7:1509–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez M, Malagoli P, Vernay A, Améglio T, Balandier P (2020) Below-ground nitrogen transfer from oak seedlings facilitates Molinia growth: 15N pulse-chase labelling. Plant Soil 20:1–4

    Google Scholar 

  • Franklin O, Cambui CA, Gruffman L, Palmroth S, Oren R, Näsholm T (2017) The carbon bonus of organic nitrogen enhances nitrogen use efficiency of plants. Plant Cell Environ 40:25–35

    Article  CAS  PubMed  Google Scholar 

  • Frey SD (2019) Mycorrhizal fungi as mediators of soil organic matter dynamics. Ann Rev Ecol Evol Syst 50:237–259

    Article  Google Scholar 

  • Frey-Klett P, Garbaye JA, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  CAS  PubMed  Google Scholar 

  • Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty PE (2016) Take a trip through the plant and fungal transportome of mycorrhiza. Trends Plant Sci 21:937–950

    Article  CAS  PubMed  Google Scholar 

  • Garg N, Chandel S (2011) Effect of mycorrhizal inoculation on growth, nitrogen fixation, and nutrient uptake in Cicer arietinum (L.) under salt stress. Turk J Agric For 35:205–214

    CAS  Google Scholar 

  • Gojon A (2017) Nitrogen nutrition in plants: rapid progress and new challenges. J Exp Bot 68:2457–2462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? Eur J Soil Sci 57:2–12

    Article  Google Scholar 

  • Gui H, Purahong W, Hyde KD, Xu J, Mortimer PE (2017) The arbuscular mycorrhizal fungus Funneliformis mosseae alters bacterial communities in subtropical forest soils during litter decomposition. Front Microbiol 8:1120. https://doi.org/10.3389/fmicb.2017.01120

    Article  PubMed  PubMed Central  Google Scholar 

  • Hack CM, Porta M, Schäufele R, Grimoldi AA (2019) Arbuscular mycorrhiza mediated effects on growth, mineral nutrition and biological nitrogen fixation of Melilotus alba Med. in a subtropical grassland soil. Appl Soil Ecol 134:38–44

    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

    Article  CAS  Google Scholar 

  • Han J, Shi J, Zeng L, Xu J, Wu L (2015) Effects of nitrogen fertilization on the acidity and salinity of greenhouse soils. Environ Sci Pollut Res 22:2976–2986

    Article  CAS  Google Scholar 

  • Hao Z, Xie W, Jiang X, Wu Z, Zhang X, Chen B (2019) Arbuscular mycorrhizal fungus improves RhizobiumGlycyrrhiza seedling symbiosis under drought stress. Agronomy 9:572. https://doi.org/10.3390/agronomy9100572

    Article  CAS  Google Scholar 

  • Hawkins HJ, George E (2001) Reduced 15N nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium vs. nitrate nutrition. Ann Bot 87:303–311

    Article  CAS  Google Scholar 

  • Hawkins BJ, Robbins S (2010) pH affects ammonium, nitrate and proton fluxes in the apical region of conifer and soybean roots. Physiol Plant 138:238–247

    Article  CAS  PubMed  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

    Article  CAS  Google Scholar 

  • He X, Xu M, Qiu GY, Zhou J (2009) Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. J Plant Ecol 2:107–118

    Article  Google Scholar 

  • He S, Long M, He X, Guo L, Yang J, Yang P, Hu T (2017) Arbuscular mycorrhizal fungi and water availability affect biomass and C: N: P ecological stoichiometry in alfalfa (Medicago sativa L.) during regrowth. Acta Physiol Plant 39:199. https://doi.org/10.1007/s11738-017-2493-7

    Article  Google Scholar 

  • He Y, Cornelissen JH, Wang P, Dong M, Ou J (2019) Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environ Sci Pollut Res 26:8828–8837

    Article  CAS  Google Scholar 

  • Herdler S, Kreuzer K, Scheu S, Bonkowski M (2008) Interactions between arbuscular mycorrhizal fungi (Glomus intraradices, Glomeromycota) and amoebae (Acanthamoeba castellanii, Protozoa) in the rhizosphere of rice (Oryza sativa). Soil Biol Biochem 40:660–668

    Article  CAS  Google Scholar 

  • Herman DJ, Firestone MK, Nuccio E, Hodge A (2012) Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. FEMS Microbiol Ecol 80:236–247

    Article  CAS  PubMed  Google Scholar 

  • Hestrin R, Hammer EC, Mueller CW, Lehmann J (2019) Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun Biol 2:1–9

    Article  CAS  Google Scholar 

  • Hino T, Matsumoto Y, Nagano S, Sugimoto H, Fukumori Y, Murata T, Iwata S, Shiro Y (2010) Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330:1666–1670

    Article  CAS  PubMed  Google Scholar 

  • Hodge A (2014) Interactions between arbuscular mycorrhizal fungi and organic material substrates. Adv Appl Microbiol 89:47–99

    Article  PubMed  Google Scholar 

  • Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273

    Article  Google Scholar 

  • Hsu SF, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3:124–136

    Article  CAS  PubMed  Google Scholar 

  • Ingraffia R, Amato G, Frenda AS, Giambalvo D (2019) Impacts of arbuscular mycorrhizal fungi on nutrient uptake, N2 fixation, N transfer, and growth in a wheat/faba bean intercropping system. PLoS One 14:e0213672. https://doi.org/10.1371/journal.pone.0213672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inselsbacher E, Näsholm T (2012) The below-ground perspective of forest plants: soil provides mainly organic nitrogen for plants and mycorrhizal fungi. New Phytol 195:329–334

    Article  CAS  PubMed  Google Scholar 

  • Jansa J, Gryndler M (2010) Biotic environment of the arbuscular mycorrhizal fungi in soil. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Heidelberg, pp 209–236

    Chapter  Google Scholar 

  • Jansa J, Bukovská P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts–or just soil free-riders? Front Plant Sci 4:134. https://doi.org/10.3389/fpls.2013.00134

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin H (2009) Arginine bi-directional translocation and breakdown into ornithine along the arbuscular mycorrhizal mycelium. Sci China Ser C 52:381–389

    Article  CAS  Google Scholar 

  • Jin H, Liu J, Liu J, Huang X (2012) Forms of nitrogen uptake, translocation, and transfer via arbuscular mycorrhizal fungi: a review. Sci China Life Sci 55:474–482

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Wilson GW, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484

    Article  CAS  PubMed  Google Scholar 

  • Kandhasamy N, Ravichandran KR, Thangavelu M (2020) Interactive influence of soil and plant genotypes on mycorrhizal dependency in finger millet. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-020-00212-2

  • Klironomos JN, Allen MF, Rillig MC, Piotrowski J, Makvandi-Nejad S, Wolfe BE, Powell JR (2005) Abrupt rise in atmospheric CO2 overestimates community response in a model plant–soil system. Nature 433:621–624

    Article  CAS  PubMed  Google Scholar 

  • Kobae Y (2019) Dynamic phosphate uptake in arbuscular mycorrhizal roots under field conditions. Front Environ Sci 6:159. https://doi.org/10.3389/fenvs.2018.00159

    Article  Google Scholar 

  • Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415

    Article  CAS  PubMed  Google Scholar 

  • Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211

    Article  CAS  PubMed  Google Scholar 

  • Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95:1045–1054

    Article  PubMed  Google Scholar 

  • Leifheit EF, Verbruggen E, Rillig MC (2014) Rotation of hyphal in-growth cores has no confounding effects on soil abiotic properties. Soil Biol Biochem 79:78–80

    Article  CAS  Google Scholar 

  • Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    Article  CAS  PubMed  Google Scholar 

  • Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci U S A 104:11192–11196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ran W, Zhang R, Sun S, Xu G (2009) Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mung bean intercropping system. Plant Soil 315:285–296

    Article  CAS  Google Scholar 

  • Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci U S A 113:6496–6501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liese R, Lübbe T, Albers NW, Meier IC (2018) The mycorrhizal type governs root exudation and nitrogen uptake of temperate tree species. Tree Physiol 38:83–95

    Article  CAS  PubMed  Google Scholar 

  • Lin J, Wang Y, Sun S, Mu C, Yan X (2017) Effects of arbuscular mycorrhizal fungi on the growth, photosynthesis and photosynthetic pigments of Leymus chinensis seedlings under salt-alkali stress and nitrogen deposition. Sci Total Environ 576:234–241

    Article  CAS  PubMed  Google Scholar 

  • Lindsay PL, Williams BN, MacLean A, Harrison MJ (2019) A phosphate-dependent requirement for transcription factors IPD3 and IPD3L during arbuscular mycorrhizal symbiosis in Medicago truncatula. Mol Plant-Microbe Interact 32:1277–1290

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Song F, Liu S, Li X, Liu F, Zhu X (2019) Arbuscular mycorrhiza improves nitrogen use efficiency in soybean grown under partial root-zone drying irrigation. Arch Agron Soil Sci 65:269–279

    Article  CAS  Google Scholar 

  • Liu J, Chen J, Xie K, Tian Y, Yan A, Liu J, Huang Y, Wang S, Zhu Y, Chen A, Xu G (2020) A mycorrhiza-specific H+-ATPase is essential for arbuscule development and symbiotic phosphate and nitrogen uptake. Plant Cell Environ 43:1069–1108

    Article  CAS  PubMed  Google Scholar 

  • López-Gutiérrez JC, Henry S, Hallet S, Martin-Laurent F, Catroux G, Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Meth 57:399–407

    Article  CAS  Google Scholar 

  • Lu JK, Li ZS, Yang FC, Wang SK, Liang JF, He XH (2020) Concurrent carbon and nitrogen transfer between hemiparasite Santalum album and two N2-fixing hosts in a sandalwood plantation. Forest Ecol Manag 464:118060. https://doi.org/10.1016/j.foreco.2020.118060

    Article  Google Scholar 

  • Mackay JE, Macdonald LM, Smernik RJ, Cavagnaro TR (2017) Organic amendments as phosphorus fertilisers: chemical analyses, biological processes and plant P uptake. Soil Biol Biochem 107:50–59

    Article  CAS  Google Scholar 

  • Marschner H (2011) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, London

    Google Scholar 

  • Marschner P, Timonen S (2006) Bacterial community composition and activity in rhizosphere of roots colonized by arbuscular mycorrhizal fungi. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizosphere. Soil biology, vol 7. Springer, Berlin, pp 139–154

    Chapter  Google Scholar 

  • Masson-Boivin C, Sachs JL (2018) Symbiotic nitrogen fixation by rhizobia—the roots of a success story. Curr Opin Plant Biol 44:7–15

    Article  CAS  PubMed  Google Scholar 

  • Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:339. https://doi.org/10.3389/fpls.2015.00339

    Article  PubMed  PubMed Central  Google Scholar 

  • Míguez-Montero MA, Valentine A, Pérez-Fernández MA (2020) Regulatory effect of phosphorus and nitrogen on nodulation and plant performance of leguminous shrubs. AoB Plants 12:plz047. https://doi.org/10.1093/aobpla/plz047

    Article  CAS  Google Scholar 

  • Mohammadi M, Modarres-Sanavy SA, Pirdashti H, Zand B, Tahmasebi-Sarvestani Z (2019) Arbuscular mycorrhizae alleviate water deficit stress and improve antioxidant response, more than nitrogen fixing bacteria or chemical fertilizer in the evening primrose. Rhizosphere 9:76–89

    Article  Google Scholar 

  • Molla MN, Solaiman AR (2009) Association of arbuscular mycorrhizal fungi with leguminous crops grown in different agro-ecological zones of Bangladesh. Arch Agron Soil Sci 55:233–245

    Article  CAS  Google Scholar 

  • Montenegro-Gómez SP, Gómez-Posada S, Barrera-Berdugo SE (2017) Effect of poultry manure on Azotobacter sp., Azospirillum sp. and arbuscular mycorrhizal fungi in anion culture (A. fistulosum). Entramado 13:250–257

    Article  Google Scholar 

  • Montesinos-Navarro A, Verdú M, Querejeta JI, Sortibrán L, Valiente-Banuet A (2016) Soil fungi promote nitrogen transfer among plants involved in long-lasting facilitative interactions. Perspect Plant Ecol Evol Syst 18:45–51

    Article  Google Scholar 

  • Morgan JB, Connolly EL (2013) Plant-soil interactions: nutrient uptake. Nat Educ Knowl 4:2

    Google Scholar 

  • Mrkovacki N, Milic V (2001) Use of Azotobacter chroococcum as potentially useful in agricultural application. Ann Microbiol 51:145–158

    Google Scholar 

  • Mus F, Crook MB, Garcia K, Costas AG, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GE, Poole PS, Udvardi MK (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Musyoka DM, Njeru EM, Nyamwange MM, Maingi JM (2020) Arbuscular mycorrhizal fungi and Bradyrhizobium co-inoculation enhances nitrogen fixation and growth of green grams (Vigna radiata L.) under water stress. J Plant Nutr 43:1036–1047

    Article  CAS  Google Scholar 

  • Nannipieri P, Eldor P (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369

    Article  CAS  Google Scholar 

  • Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48

    Article  PubMed  CAS  Google Scholar 

  • Norman JS, Friesen ML (2017) Complex N acquisition by soil diazotrophs: how the ability to release exoenzymes affects N fixation by terrestrial free-living diazotrophs. ISME J 11:315–326

    Article  CAS  PubMed  Google Scholar 

  • Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881

    Article  CAS  PubMed  Google Scholar 

  • Nygren P, Leblanc HA (2015) Dinitrogen fixation by legume shade trees and direct transfer of fixed N to associated cacao in a tropical agroforestry system. Tree Physiol 35:134–147

    Article  CAS  PubMed  Google Scholar 

  • Obertello M, Wall LG (2015) Interactions between Frankia BCU110501 (actinorhiza) and Gigaspora rosea (arbuscular mycorrhiza) with Discaria trinervis studied by spot inoculation. Symbiosis 66:13–20

    Article  Google Scholar 

  • Okiobe ST, Augustin J, Veresoglou SD (2019) Disentangling direct and indirect effects of mycorrhiza on nitrous oxide activity and denitrification. Soil Biol Biochem 134:142–151

    Article  CAS  Google Scholar 

  • Okiobe ST, Rillig MC, Mola M, Augustin J, Parolly G, Veresoglou SD (2020) Arbuscular mycorrhiza has little influence on N2O potential emissions compared to plant diversity in experimental plant communities. FEMS Microbiol Ecol 96:fiz208. https://doi.org/10.1093/femsec/fiz208

    Article  CAS  PubMed  Google Scholar 

  • Ortas I, Iqbal T, Yücel YC (2019) Mycorrhizae enhances horticultural plant yield and nutrient uptake under phosphorus deficient field soil condition. J Plant Nutr 42:1152–1164

    Article  CAS  Google Scholar 

  • Paterson E, Sim A, Davidson J, Daniell TJ (2016) Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralisation. Plant Soil 408:243–254

    Article  CAS  Google Scholar 

  • Pérez-Fernández MA, Calvo-Magro E, Rodríguez-Sánchez J, Valentine A (2017) Differential growth costs and nitrogen fixation in Cytisus multiflorus (L’Hér.) Sweet and Cytisus scoparius (L.) Link are mediated by sources of inorganic. N Plant Biol 19:742–748

    Article  PubMed  CAS  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51

    Article  CAS  PubMed  Google Scholar 

  • Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J (2016) Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol 6:4332–4346

    Article  PubMed  PubMed Central  Google Scholar 

  • Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J (2017) Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci 8:390. https://doi.org/10.3389/fpls.2017.00390

    Article  PubMed  PubMed Central  Google Scholar 

  • Quilliam RS, Marsden KA, Gertler C, Rousk J, DeLuca TH, Jones DL (2012) Nutrient dynamics, microbial growth and weed emergence in biochar amended soil are influenced by time since application and reapplication rate. Agric Ecosyst Environ 158:192–199

    Article  CAS  Google Scholar 

  • Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222

    CAS  Google Scholar 

  • Rodriguez C, Carlsson G, Englund JE, Flöhr A, Pelzer E, Jeuffroy MH, Makowski D, Jensen ES (2020) Grain legume-cereal intercropping enhances the use of soil-derived and biologically fixed nitrogen in temperate agroecosystems. A meta-analysis. Eur J Agron 118:126077. https://doi.org/10.1016/j.eja.2020.126077

    Article  CAS  Google Scholar 

  • Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J 3:675–684

    Article  CAS  PubMed  Google Scholar 

  • Rosolem CA, Ritz K, Cantarella H, Galdos MV, Hawkesford MJ, Whalley WR, Mooney SJ (2017) Enhanced plant rooting and crop system management for improved N use efficiency. In: Sparks DL (ed) Advances in agronomy, vol 146. Academic Press, Cambridge, pp 205–239

    Google Scholar 

  • Rydlová J, Püschel D, Dostálová M, Janoušková M, Frouz J (2016) Nutrient limitation drives response of Calamagrostis epigejos to arbuscular mycorrhiza in primary succession. Mycorrhiza 26:757–767

    Article  PubMed  CAS  Google Scholar 

  • Sabannavar SJ, Lakshman HC (2011) Synergistic interactions among Azotobacter, Pseudomonas, and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. Commun Soil Sci Plant Anal 42:2122–2133

    Article  CAS  Google Scholar 

  • Sabatino L, Iapichino G, Consentino BB, D’Anna F, Rouphael Y (2020) Root stock and arbuscular mycorrhiza combinatorial effects on eggplant crop performance and fruit quality under greenhouse conditions. Agronomy 1:693. https://doi.org/10.3390/agronomy10050693

    Article  CAS  Google Scholar 

  • Saharan K, Schütz L, Kahmen A, Wiemken A, Boller T, Mathimaran N (2018) Finger millet growth and nutrient uptake is improved in intercropping with pigeon pea through biofertilization and bioirrigation mediated by arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria. Front Environ Sci 6:46. https://doi.org/10.3389/fenvs.2018.00046

    Article  Google Scholar 

  • Saia S, Benítez E, García-Garrido JM, Settanni L, Amato G, Giambalvo D (2014) The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. J Agric Sci 152:370–378

    Article  Google Scholar 

  • Scandellari F (2017) Arbuscular mycorrhizal contribution to nitrogen uptake of grapevines. Vitis 56:147–154

    CAS  Google Scholar 

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Seguel A, Barea JM, Cornejo P, Borie F (2015) Role of arbuscular mycorrhizal symbiosis in phosphorus-uptake efficiency and aluminium tolerance in barley growing in acid soils. Crop Pasture Sci 66:696–705

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storer K, Coggan A, Ineson P, Hodge A (2018) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 220:1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Tran LS (2004) Symbiotic nitrogen fixation in legume nodules: metabolism and regulatory mechanisms. Int J Mol Sci 15:19389–19393

    Article  CAS  Google Scholar 

  • Sun Z, Song J, Xin XA, Xie X, Zhao B (2018) Arbuscular mycorrhizal fungal 14-3-3 proteins are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis. Front Microbiol 9:91. https://doi.org/10.3389/fmicb.2018.00091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Symanczik S, Lehmann MF, Wiemken A, Boller T, Courty PE (2018) Effects of two contrasted arbuscular mycorrhizal fungal isolates on nutrient uptake by Sorghum bicolor under drought. Mycorrhiza 28:779–785

    Article  CAS  PubMed  Google Scholar 

  • Talaat NB, Shawky BT (2014) Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 98:20–31

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Tang Z, Xu W, Zhou G, Bai Y, Li J, Tang X, Chen D, Liu Q, Ma W, Xiong G, He H (2018) Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems. Proc Natl Acad Sci U S A 115:4033–4038

    Article  PubMed  PubMed Central  Google Scholar 

  • Tavarini S, Passera B, Martini A, Avio L, Sbrana C, Giovannetti M, Angelini LG (2018) Plant growth, steviol glycosides and nutrient uptake as affected by arbuscular mycorrhizal fungi and phosphorous fertilization in Stevia rebaudiana Bert. Ind Crop Prod 111:899–907

    Article  CAS  Google Scholar 

  • Taylor MK, Lankau RA, Wurzburger N (2016) Mycorrhizal associations of trees have different indirect effects on organic matter decomposition. J Ecol 104:1576–1584

    Article  CAS  Google Scholar 

  • Teutscherova N, Vazquez E, Arango J, Arevalo A, Benito M, Pulleman M (2019) Native arbuscular mycorrhizal fungi increase the abundance of ammonia-oxidizing bacteria, but suppress nitrous oxide emissions shortly after urea application. Geoderma 338:493–501

    Article  CAS  Google Scholar 

  • Thilakarathna MS, McElroy MS, Chapagain T, Papadopoulos YA, Raizada MN (2016) Belowground nitrogen transfer from legumes to non-legumes under managed herbaceous cropping systems. A review. Agron Sustain Dev 36:58. https://doi.org/10.1007/s13593-016-0396-4

    Article  CAS  Google Scholar 

  • Thirkell TJ, Cameron DD, Hodge A (2016) Resolving the ‘nitrogen paradox’ of arbuscular mycorrhizas: fertilization with organic matter brings considerable benefits for plant nutrition and growth. Plant Cell Environ 39:1683–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian C, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y (2010) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  CAS  PubMed  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Tomè E, Tagliavini M, Scandellari F (2015) Recently fixed carbon allocation in strawberry plants and concurrent inorganic nitrogen uptake through arbuscular mycorrhizal fungi. J Plant Physiol 179:83–89

    Article  PubMed  CAS  Google Scholar 

  • Tonhauzer K, Tonhauzer P, Szemesová J, Šiška B (2020) Estimation of N2O emissions from agricultural soils and determination of nitrogen leakage. Atmos 11:552. https://doi.org/10.3390/atmos11060552

    Article  CAS  Google Scholar 

  • Torres-Olivar V, Villegas-Torres OG, Domínguez-Patiño ML, Sotelo-Nava H, Rodríguez-Martínez A, Melgoza-Alemán RM, Valdez-Aguilar LA, Alia-Tejacal I (2014) Role of nitrogen and nutrients in crop nutrition. J Agric Sci Techol B 4:29–37

    Google Scholar 

  • Toussaint JP, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can J Microbiol 50:251–260

    Article  CAS  PubMed  Google Scholar 

  • Trap J, Bonkowski M, Plassard C, Villenave C, Blanchart E (2016) Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398:1–24

    Article  CAS  Google Scholar 

  • Ueda MU, Kachina P, Marod D, Nakashizuka T, Kurokawa H (2017) Soil properties and gross nitrogen dynamics in old growth and secondary forest in four types of tropical forest in Thailand. Forest Ecol Manag 398:130–139

    Article  Google Scholar 

  • Valentine AJ, Osborne BA, Mitchell DT (2002) Form of inorganic nitrogen influences mycorrhizal colonisation and photosynthesis of cucumber. Sci Hortic 92:229–239

    Article  CAS  Google Scholar 

  • Vallorani L, Polidori E, Sacconi C, Agostini D, Pierleoni R, Piccoli G, Zeppa S, Stocchi V (2002) Biochemical and molecular characterization of NADP-glutamate dehydrogenase from the ectomycorrhizal fungus Tuber borchii. New Phytol 154:779–790

    Article  CAS  PubMed  Google Scholar 

  • Van Aarle IM, Olsson PA (2008) Resource partitioning between extraradical and intraradical AM fungal mycelium. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, ecophysiology, structure and systematics, 3rd edn. Springer, Heidelberg, pp 321–336

    Google Scholar 

  • Vangelisti A, Natali L, Bernardi R, Sbrana C, Turrini A, Hassani-Pak K, Hughes D, Cavallini A, Giovannetti M, Giordani T (2018) Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots. Sci Rep 8:1–4

    Article  CAS  Google Scholar 

  • Varinderpal-Singh SS, Kunal GSK, Choudhary R, Singh R, Adholeya A, Bijay-Singh (2020) Synergistic use of plant growth-promoting rhizobacteria, arbuscular mycorrhizal fungi, and spectral properties for improving nutrient use efficiencies in wheat (Triticum aestivum L.). Commun Soil Sci Plant Anal 5:14–27

    Article  CAS  Google Scholar 

  • Verbruggen E, van der Heijden MG, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109

    Article  PubMed  Google Scholar 

  • Veresoglou SD, Sen R, Mamolos AP, Veresoglou DS (2011) Plant species identity and arbuscular mycorrhizal status modulate potential nitrification rates in nitrogen-limited grassland soils. J Ecol 99:1339–1349

    Article  CAS  Google Scholar 

  • Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62

    Article  CAS  Google Scholar 

  • Vergara C, Araujo KEC, Souza SR, Schultz N, Saggin Junior OJ, Sperandio MVL, Zilli JE (2019) Plant-mycorrhizal fungi interaction and response to inoculation with different growth-promoting fungi. Pesq Agropec Bras 54:1–24

    Article  Google Scholar 

  • Verzeaux J, Hirel B, Dubois F, Lea PJ, Tétu T (2017) Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Sci 264:48–56

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Sheng L, Zhao D, Sheng J, Wang X, Liao H (2016) Allocation of nitrogen and carbon is regulated by nodulation and mycorrhizal networks in soybean/maize intercropping system. Front Plant Sci 7:1901. https://doi.org/10.3389/fpls.2016.01901

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang M, Li Y, Wu A, Huang J (2018) Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 13:e0196408. https://doi.org/10.1371/journal.pone.0196408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whiteside MD, Digman MA, Gratton E, Treseder KK (2012a) Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biol Biochem 55:7–13

    Article  CAS  Google Scholar 

  • Whiteside MD, Garcia MO, Treseder KK (2012b) Amino acid uptake in arbuscular mycorrhizal plants. PLoS One 7:e47643. https://doi.org/10.1371/journal.pone.0047643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu F, Zhang H, Fang F, Liu H, Tang M (2017) Arbuscular mycorrhizal fungi alter nitrogen allocation in the leaves of Populus× canadensis ‘Neva’. Plant Soil 421:477–491

    Article  CAS  Google Scholar 

  • Wu F, Fang F, Wu N, Li L, Tang M (2020) Nitrate transporter gene expression and kinetics of nitrate uptake by Populus× canadensis ‘Neva’ in relation to arbuscular mycorrhizal fungi and nitrogen availability. Front Microbiol 11:176. https://doi.org/10.3389/fmicb.2020.00176

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu L, Cheng S, Fang H, Xin X, Xu X, Tang H (2019) Soil inorganic nitrogen composition and plant functional type determine forage crops nitrogen uptake preference in the temperate cultivated grassland, Inner Mongolia. Soil Sci Plant Nutr 65:501–510

    Article  Google Scholar 

  • Yang H, Zhou J, Weih M, Li Y, Zhai S, Zhang Q, Chen W, Liu J, Liu L, Hu S (2020) Mycorrhizal nitrogen uptake of wheat is increased by earthworm activity only under no-till and straw removal conditions. Appl Soil Ecol 155:103672. https://doi.org/10.1016/j.apsoil.2020.103672

    Article  Google Scholar 

  • Yu Z, Xu J, Liu S, Hu L, Ren M, Liu Y, Tang J, Chen X (2020) Adult plants facilitate their conspecific seedlings by enhancing arbuscular mycorrhizae in a saline soil. Plant Soil 447:333–345

    Article  CAS  Google Scholar 

  • Zarea MJ, Karimi N, Goltapeh EM, Ghalavand A (2011) Effect of cropping systems and arbuscular mycorrhizal fungi on soil microbial activity and root nodule nitrogenase. J Saudi Soc Agri Sci 10:109–120

    CAS  Google Scholar 

  • Zhang H, Wang X, Gao Y, Sun B (2020) Short-term N transfer from alfalfa to maize is dependent more on arbuscular mycorrhizal fungi than root exudates in N deficient soil. Plant Soil 446:23–41

    Article  CAS  Google Scholar 

  • Zhu X, Song F, Liu S, Liu F (2016) Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2. Mycorrhiza 26:133–140

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Koshila Ravi, R., Balachandar, M., Yuvarani, S., Anaswara, S., Pavithra, L., Muthukumar, T. (2021). Arbuscular Mycorrhiza in Sustainable Plant Nitrogen Nutrition: Mechanisms and Impact. In: Cruz, C., Vishwakarma, K., Choudhary, D.K., Varma, A. (eds) Soil Nitrogen Ecology. Soil Biology, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-030-71206-8_21

Download citation

Publish with us

Policies and ethics