Advertisement

Arbuscular mycorrhiza: a viable strategy for soil nutrient loss reduction

  • Manoj PariharEmail author
  • Vijay Singh Meena
  • Pankaj Kumar Mishra
  • Amitava Rakshit
  • Mahipal Choudhary
  • Ram Prakash Yadav
  • Kiran Rana
  • Jaideep Kumar Bisht
Mini-Review
  • 31 Downloads

Abstract

Arbuscular mycorrhiza fungi’s (AMF) role in plant nutrition and stress management is well known, but very few researches and studies have been conducted so far on the fungal ability to reduce different nutrient losses (runoff, leaching and volatilization) from the soil system. This important ecosystem service of AMF had been neglected largely. From the recent findings, it has been confirmed that mycorrhizal symbiosis has potential to check the losses of applied nutrients. The role of soil biota in nutrient cycling is indispensable and determines the nutrient availability to plants. Among these biota, AMF’s association with plants is the most prevalent, but the exact mechanisms followed by AMF in nutrient cycling, transformation and reducing nutrient loss ability are still inconclusive. In this review, we will try to unlock this particular aspect of AMF which is important to achieve global food demand in a sustainable way.

Keywords

AM fungi Nutrient use efficiency Nutrient losses Nutrient cycling 

Notes

Acknowledgements

We are thankful to ICAR-VPKAS, Almora and Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University for their constructive comments and suggestions, which helped us to improve this manuscript.

References

  1. Adiova JM, Pampolina NM, Aggangan NS (2013) Effect of arbuscular mycorrhizal fungi inoculation on growth and Cu uptake and toxicity of Desmodium cinereum (Kunth) DC. Philipp J Sci 142:87–96Google Scholar
  2. Albertsen A, Ravnskov S, Green H et al (2006) Interactions between the external mycelium of the mycorrhizal fungus Glomus intraradices and other soil microorganisms as affected by organic matter. Soil Biol Biochem 38:1008–1014.  https://doi.org/10.1016/J.SOILBIO.2005.08.015 CrossRefGoogle Scholar
  3. Allen MR, Barros VR, Broome J et al (2014) IPCC fifth assessment synthesis report-climate change 2014 synthesis reportGoogle Scholar
  4. Amora-Lazcano E, Vázquez MM, Azcón R (1998) Response of nitrogen-transforming microorganisms to arbuscular mycorrhizal fungi. Biol Fertil Soils 27:65–70.  https://doi.org/10.1007/s003740050401 CrossRefGoogle Scholar
  5. An G-H, Kobayashi S, Enoki H et al (2010) How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil 327:441–453.  https://doi.org/10.1007/s11104-009-0073-3 CrossRefGoogle Scholar
  6. Arines J, Vilarino A, Sainz M (1989) Effect of different inocula of vesicular-arbuscular mycorrhizal fungi on manganese content and concentration in red clover (Trifolium pratense L.) plants. New Phytol 112:215–219CrossRefGoogle Scholar
  7. Arines J, Porto ME, Vilariño A (1992) Effect of manganese on vesicular-arbuscular mycorrhizal development in red clover plants and on soil Mn-oxidizing bacteria. Mycorrhiza 1:127–131.  https://doi.org/10.1007/BF00203260 CrossRefGoogle Scholar
  8. Aryal UK, Xu HL, Fujita M (2003) Rhizobia and AM fungal inoculation improve growth and nutrient uptake of bean plants under organic fertilization. J Sustain Agric 21:27–39.  https://doi.org/10.1300/J064v21n03_04 CrossRefGoogle Scholar
  9. Asghari HR, Cavagnaro TR (2012) Arbuscular mycorrhizas reduce nitrogen loss via leaching. PLoS One 7:e29825.  https://doi.org/10.1371/journal.pone.0029825 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Asghari HR, Chittleborough DJ, Smith FA, Smith SE (2005) Influence of arbuscular mycorrhizal (AM) symbiosis on phosphorus leaching through soil cores. Plant Soil 275:181–193.  https://doi.org/10.1007/s11104-005-1328-2 CrossRefGoogle Scholar
  11. Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246.  https://doi.org/10.1007/s00572-008-0215-0 CrossRefPubMedGoogle Scholar
  12. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42.  https://doi.org/10.1007/s005720100097 CrossRefGoogle Scholar
  13. Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381.  https://doi.org/10.4141/S04-002 CrossRefGoogle Scholar
  14. Avrahami S, Bohannan BJM (2007) Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173.  https://doi.org/10.1128/AEM.01803-06 CrossRefPubMedGoogle Scholar
  15. Azcón R, Ruiz-Lozano JM, Rodríguez R (2001) Differential contribution of arbuscular mycorrhizal fungi to plant nitrate uptake (15N) under increasing N supply to the soil. Can J Bot 79:1175–1180.  https://doi.org/10.1139/b01-093 CrossRefGoogle Scholar
  16. Baar J (2010) Development of soil quality metrics using mycorrhizal fungi. Span J Agric Res 8:137.  https://doi.org/10.5424/sjar/201008S1-1233 CrossRefGoogle Scholar
  17. Beauregard MS, Gauthier M-P, Hamel C et al (2013) Various forms of organic and inorganic P fertilizers did not negatively affect soil- and root-inhabiting AM fungi in a maize–soybean rotation system. Mycorrhiza 23:143–154.  https://doi.org/10.1007/s00572-012-0459-6 CrossRefPubMedGoogle Scholar
  18. Bender SF, van der Heijden MGA (2015) Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J Appl Ecol 52:228–239.  https://doi.org/10.1111/1365-2664.12351 CrossRefGoogle Scholar
  19. Bender SF, Plantenga F, Neftel A et al (2014) Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J 8:1336–1345.  https://doi.org/10.1038/ismej.2013.224 CrossRefPubMedGoogle Scholar
  20. Bender SF, Conen F, Van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem 80:283–292.  https://doi.org/10.1016/j.soilbio.2014.10.016 CrossRefGoogle Scholar
  21. Berks BC, Ferguson SJ, Moir JWB, Richardson DJ (1995) Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta Bioenergetics 1232:97–173.  https://doi.org/10.1016/0005-2728(95)00092-5 CrossRefGoogle Scholar
  22. Bharadwaj DP, Alström S, Lundquist PO (2012) Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions. Mycorrhiza 22:437–447.  https://doi.org/10.1007/s00572-011-0418-7 CrossRefPubMedGoogle Scholar
  23. Bolan NS, Robson AD, Barrow NJ (1987) Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant Soil 99:401–410.  https://doi.org/10.1007/BF02370885 CrossRefGoogle Scholar
  24. Borie F, Rubio R, Rouanet JL et al (2006) Effects of tillage systems on soil characteristics, glomalin and mycorrhizal propagules in a Chilean Ultisol. Soil Tillage Res 88:253–261.  https://doi.org/10.1016/J.STILL.2005.06.004 CrossRefGoogle Scholar
  25. Borie F, Rubio R, Morales A (2008) Arbuscular mycorrhizal fungi and soil aggregation Hongos micorrícicos arbusculares y agregación de suelo. J Soil Sci Plant Nutr 8:9–18Google Scholar
  26. Börstler B, Renker C, Kahmen A, Buscot F (2006) Species composition of arbuscular mycorrhizal fungi in two mountain meadows with differing management types and levels of plant biodiversity. Biol Fertil Soils 42:286–298.  https://doi.org/10.1007/s00374-005-0026-9 CrossRefGoogle Scholar
  27. Bowles TM, Jackson LE, Cavagnaro TR (2018) Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob Change Biol 24:e171–e182.  https://doi.org/10.1111/gcb.13884 CrossRefGoogle Scholar
  28. Butterbach-Bahl K, Baggs EM, Dannenmann M et al (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc Lond B Biol Sci 368:20130122.  https://doi.org/10.1098/rstb.2013.0122 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Canadell JG, Schulze ED (2014) Global potential of biospheric carbon management for climate mitigation. Nat Commun 5:5282.  https://doi.org/10.1038/ncomms6282 CrossRefPubMedGoogle Scholar
  30. Carmo M, García-Ruiz R, Ferreira MI, Domingos T (2017) The N–P–K soil nutrient balance of Portuguese cropland in the 1950s: the transition from organic to chemical fertilization. Sci Rep 7:8111.  https://doi.org/10.1038/s41598-017-08118-3 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Carpio LA, Davies FT, Arnold MA (2005) Arbuscular mycorrhizal fungi, organic and inorganic controlled-release fertilizers: effect on growth and leachate of container-grown bush morning glory (Ipomoea carnea ssp. fistulosa) under high production temperatures. J Am Soc Hortic Sci 130(1):131–139CrossRefGoogle Scholar
  32. Castillo CG, Rubio R, Rouanet JL, Borie F (2006) Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an Ultisol. Biol Fertil Soils 43:83–92.  https://doi.org/10.1007/s00374-005-0067-0 CrossRefGoogle Scholar
  33. Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325.  https://doi.org/10.1007/s11104-008-9559-7 CrossRefGoogle Scholar
  34. Cavagnaro TR, Jackson LE, Six J et al (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225.  https://doi.org/10.1007/s11104-005-5847-7 CrossRefGoogle Scholar
  35. Cavagnaro TR, Gleadow RM, Miller RE (2011) Plant nutrient acquisition and utilisation in a high carbon dioxide world. Funct Plant Biol 38:87.  https://doi.org/10.1071/FP10124 CrossRefGoogle Scholar
  36. 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.  https://doi.org/10.1007/s11104-011-1021-6 CrossRefGoogle Scholar
  37. Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290.  https://doi.org/10.1016/j.tplants.2015.03.004 CrossRefPubMedGoogle Scholar
  38. Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491.  https://doi.org/10.1016/J.TPLANTS.2013.05.001 CrossRefPubMedGoogle Scholar
  39. Chen B, Shen H, Li X et al (2004) Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant Soil 261:219–229.  https://doi.org/10.1023/B:PLSO.0000035538.09222.ff CrossRefGoogle Scholar
  40. Cheng L, Booker FL, Tu C et al (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science (New York, NY) 337:1084–1087.  https://doi.org/10.1126/science.1224304 CrossRefGoogle Scholar
  41. Clark RB, Zeto SK (1996) Mineral acquisition by mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1495–1503.  https://doi.org/10.1016/S0038-0717(96)00163-0 CrossRefGoogle Scholar
  42. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902.  https://doi.org/10.1080/01904160009382068 CrossRefGoogle Scholar
  43. Clark RB, Zobel RW, Zeto SK (1999) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176.  https://doi.org/10.1007/s005720050302 CrossRefGoogle Scholar
  44. Corkidi L, Merhaut DJ, Allen EB et al (2011) Effects of mycorrhizal colonization on nitrogen and phosphorus leaching from nursery containers. HortScience 46:1472–1479CrossRefGoogle Scholar
  45. Currie WS, Aber JD (1997) Modeling leaching as a decomposition process in humid montane forests. Ecology 78:1844–1860.  https://doi.org/10.1890/0012-9658(1997)078%5b1844:MLAADP%5d2.0.CO;2 CrossRefGoogle Scholar
  46. Davidson EA, Matson PA, Vitousek PM et al (1993) Processes regulating soil emissions of NO and N2O in a seasonally dry tropical forest. Ecology 74:130–139.  https://doi.org/10.2307/1939508 CrossRefGoogle Scholar
  47. Denef K, Six J, Bossuyt H et al (2001) Influence of dry–wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics. Soil Biol Biochem 33:1599–1611.  https://doi.org/10.1016/S0038-0717(01)00076-1 CrossRefGoogle Scholar
  48. Edwards SG, Young JPW, Fitter AH (1998) Interactions between Pseudomonas fluorescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol Lett 166:297–303.  https://doi.org/10.1111/j.1574-6968.1998.tb13904.x CrossRefGoogle Scholar
  49. Faber BA, Zasoski RJ, Burau RG, Uriu K (1990) Zinc uptake by corn as affected by vesicular-arbuscular mycorrhizae. Plant Soil 129:121–130CrossRefGoogle Scholar
  50. Fellbaum CR, Mensah JA, Pfeffer PE et al (2012) 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.  https://doi.org/10.4161/psb.22015 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Fester T, Sawers R (2011) Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 30:459–470.  https://doi.org/10.1080/07352689.2011.605741 CrossRefGoogle Scholar
  52. Filion M, Starnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533.  https://doi.org/10.1046/j.1469-8137.1999.00366.x CrossRefGoogle Scholar
  53. Galván GA, Parádi I, Burger K et al (2009) Molecular diversity of arbuscular mycorrhizal fungi in onion roots from organic and conventional farming systems in the Netherlands. Mycorrhiza 19:317–328.  https://doi.org/10.1007/s00572-009-0237-2 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Gao X, Kuyper TW, Zou C et al (2007) Mycorrhizal responsiveness of aerobic rice genotypes is negatively correlated with their zinc uptake when nonmycorrhizal. Plant Soil 290:283–291.  https://doi.org/10.1007/s11104-006-9160-x CrossRefGoogle Scholar
  55. George E, Häussler K-U, Vetterlein D et al (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137.  https://doi.org/10.1139/b92-265 CrossRefGoogle Scholar
  56. Gosling P, Mead A, Proctor M et al (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556.  https://doi.org/10.1111/nph.12169 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Govindarajulu M, Pfeffer PE, Jin H et al (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823.  https://doi.org/10.1038/nature03610 CrossRefPubMedGoogle Scholar
  58. Grunwald U, Guo W, Fischer K et al (2009) Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta 229:1023–1034.  https://doi.org/10.1007/s00425-008-0877-z CrossRefPubMedPubMedCentralGoogle Scholar
  59. Hamel C (2004) Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Can J Soil Sci 84:383–395.  https://doi.org/10.4141/S04-004 CrossRefGoogle Scholar
  60. Helgason T, Merryweather JW, Denison J et al (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384.  https://doi.org/10.1046/j.1365-2745.2001.00674.x CrossRefGoogle Scholar
  61. Hesterberg D (2010) Macroscale chemical properties and X-ray absorption spectroscopy of soil phosphorus. Dev Soil Sci 34:313–356.  https://doi.org/10.1016/S0166-2481(10)34011-6 CrossRefGoogle Scholar
  62. 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.  https://doi.org/10.1073/pnas.1005874107 CrossRefPubMedGoogle Scholar
  63. Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19.  https://doi.org/10.1007/s11104-014-2162-1 CrossRefGoogle Scholar
  64. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299CrossRefPubMedGoogle Scholar
  65. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380.  https://doi.org/10.1111/j.1469-8137.1992.tb01077.x CrossRefGoogle Scholar
  66. Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488.  https://doi.org/10.1051/agro:2003013 CrossRefGoogle Scholar
  67. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Javaid A (2009) Arbuscular mycorrhizal mediated nutrition in plants. J Plant Nutr 32:1595–1618.  https://doi.org/10.1080/01904160903150875 CrossRefGoogle Scholar
  69. Jayachandran K, Hetrick BAD, Schwab AP (1992) Partitioning dissolved inorganic and organic phosphorus using acidified molybdate and isobutanol. Soil Sci Soc Am J 56:762.  https://doi.org/10.2136/sssaj1992.03615995005600030014x CrossRefGoogle Scholar
  70. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13.  https://doi.org/10.1016/j.femsec.2003.11.012 CrossRefPubMedGoogle Scholar
  71. Köhl L, Lukasiewicz CE, van der Heijden MGA (2016) Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant Cell Environ 39:136–146.  https://doi.org/10.1111/pce.12600 CrossRefPubMedGoogle Scholar
  72. Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517.  https://doi.org/10.1046/j.1469-8137.2000.00776.x CrossRefGoogle Scholar
  73. Kothari SK, Marschner H, Romheld V (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L.) in a calcareous soil. New Phytol 116:637–645.  https://doi.org/10.1111/j.1469-8137.1990.tb00549.x CrossRefGoogle Scholar
  74. Kučová L, Záhora J, Pokluda R (2016) Effect of mycorrhizal inoculation of leek Allium porrum L. on mineral nitrogen leaching. Hortic Sci 43(4):195–202.  https://doi.org/10.17221/182/2015-hortsci CrossRefGoogle Scholar
  75. Lambert DH, Weidensaul TC (1991) Element uptake by mycorrhizal soybean from sewage-sludge-treated soil. Soil Sci Soc Am J 55:393–398CrossRefGoogle Scholar
  76. Lambert DH, Baker DE, Cole H (1979) The role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Sci Soc Am J 43:976–980CrossRefGoogle Scholar
  77. Lazcano C, Barrios-Masias FH, Jackson LE (2014) Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biol Biochem 74:184–192.  https://doi.org/10.1016/J.SOILBIO.2014.03.010 CrossRefGoogle Scholar
  78. Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants—a meta-analysis. Soil Biol Biochem 69:123–131.  https://doi.org/10.1016/J.SOILBIO.2013.11.001 CrossRefGoogle Scholar
  79. Li X-L, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol 119:397–404.  https://doi.org/10.1111/j.1469-8137.1991.tb00039.x CrossRefGoogle Scholar
  80. Liu A, Hamel C, Hamilton RI et al (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336.  https://doi.org/10.1007/s005720050277 CrossRefGoogle Scholar
  81. Liu J, You L, Amini M, Obersteiner M et al (2010) A high-resolution assessment on global nitrogen flows in cropland. Proc Natl Acad Sci USA 107:8035–8040CrossRefPubMedGoogle Scholar
  82. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748.  https://doi.org/10.1126/science.1143082 CrossRefPubMedGoogle Scholar
  83. Mar Vázquez M, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272.  https://doi.org/10.1016/S0929-1393(00)00075-5 CrossRefGoogle Scholar
  84. Marschener H (1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Res 56:203–207.  https://doi.org/10.1016/S0378-4290(97)00131-7 CrossRefGoogle Scholar
  85. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  86. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102.  https://doi.org/10.1007/BF00000098 CrossRefGoogle Scholar
  87. Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274.  https://doi.org/10.1007/BF00008069 CrossRefGoogle Scholar
  88. Marschner P, Crowley D, Lieberei R (2001) Arbuscular mycorrhizal infection changes the bacterial 16S rDNA community composition in the rhizosphere of maize. Mycorrhiza 11:297–302.  https://doi.org/10.1007/s00572-001-0136-7 CrossRefPubMedGoogle Scholar
  89. Monreal CM, DeRosa M, Mallubhotla SC et al (2016) Nanotechnologies for increasing the crop use efficiency of fertilizer-micronutrients. Biol Fertil Soils 52:423–437.  https://doi.org/10.1007/s00374-015-1073-5 CrossRefGoogle Scholar
  90. Munkvold L, Kjøller R, Vestberg M et al (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364.  https://doi.org/10.1111/j.1469-8137.2004.01169.x CrossRefGoogle Scholar
  91. Ngwene B, George E, Claussen W, Neumann E (2010) Phosphorus uptake by cowpea plants from sparingly available or soluble sources as affected by nitrogen form and arbuscular-mycorrhiza-fungal inoculation. J Plant Nutr Soil Sci 173:353–359.  https://doi.org/10.1002/jpln.200900203 CrossRefGoogle Scholar
  92. Norton R, Davidson E, Roberts T (2015) Position paper - nitrogen use efficiency and nutrient performance indicators. Global Partnership on Nutrient Management (GPNM), NairobiGoogle Scholar
  93. Nye PH, Tinker PB (1977) Solute movement in the soil-root system, vol 4. University of California Press, BerkeleyGoogle Scholar
  94. Oehl F, Sieverding E, Mader P et al (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583.  https://doi.org/10.1007/s00442-003-1458-2 CrossRefPubMedGoogle Scholar
  95. Parihar M, Rakshit A (2016) Arbuscular mycorrhiza: a versatile component for alleviation of salt stress. Nat Environ Pollut Technol 15(2):417Google Scholar
  96. Parihar M, Rakshit A, Singh HB, Rana K (2018) Diversity of arbuscular mycorrhizal fungi in alkaline soils of hot sub humid ecoregion of Middle Gangetic Plains of India. Acta Agric Scand Sect B Soil Plant Sci 1:1.  https://doi.org/10.1080/09064710.2019.1582692 CrossRefGoogle Scholar
  97. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775.  https://doi.org/10.1038/nrmicro1987 CrossRefPubMedGoogle Scholar
  98. Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124.  https://doi.org/10.1007/BF00202343 CrossRefGoogle Scholar
  99. Purin S (2005) Fungos micorrízicos arbusculares: atividade, diversidade e aspectos funcionais em sistemas de produção de maçãs. Lages, Universidade do Estado de Santa Catarina (Dissertação de Mestrado)Google Scholar
  100. Rasmussen N, Lloyd DC, Ratcliffe RG et al (2000) 31P NMR for the study of P metabolism and translocation in arbuscular mycorrhizal fungi. Plant Soil 226:245–253.  https://doi.org/10.1023/A:1026411801081 CrossRefGoogle Scholar
  101. Ravnskov S, Jakobsen I (1999) Effects of Pseudomonas fluorescens DF57 on growth and P uptake of two arbuscular mycorrhizal fungi in symbiosis with cucumber. Mycorrhiza 8:329–334.  https://doi.org/10.1007/s005720050254 CrossRefGoogle Scholar
  102. Rawls WJ, Pachepsky YA, Ritchie JC et al (2003) Effect of soil organic carbon on soil water retention. Geoderma 116:61–76.  https://doi.org/10.1016/S0016-7061(03)00094-6 CrossRefGoogle Scholar
  103. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312.  https://doi.org/10.1111/j.1469-8137.2005.01558.x CrossRefPubMedGoogle Scholar
  104. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754.  https://doi.org/10.1111/j.1461-0248.2004.00620.x CrossRefGoogle Scholar
  105. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53.  https://doi.org/10.1111/j.1469-8137.2006.01750.x CrossRefPubMedGoogle Scholar
  106. Rillig MC, Mummey DL, Ramsey PW et al (2006) Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria. FEMS Microbiol Ecol 57:389–395.  https://doi.org/10.1111/j.1574-6941.2006.00129.x CrossRefPubMedGoogle Scholar
  107. Rouphael Y, Franken P, Schneider C et al (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 196:91–108.  https://doi.org/10.1016/j.scienta.2015.09.002 CrossRefGoogle Scholar
  108. Sanders FE, Tinker PB (1973) Phosphate flow into mycorrhizal roots. J Pestic Sci 4:385–395.  https://doi.org/10.1002/ps.2780040316 CrossRefGoogle Scholar
  109. Sathiyadash K, Rajendran K, Karthikeyan V, Muthukumar T (2017) Modulation of plant micronutrient uptake by arbuscular mycorrhizal fungi. Probiotics and plant health. Springer, Singapore, pp 337–352CrossRefGoogle Scholar
  110. Schlesinger WH (2009) On the fate of anthropogenic nitrogen. Proc Natl Acad Sci USA 106:203–208.  https://doi.org/10.1073/pnas.0810193105 CrossRefPubMedGoogle Scholar
  111. Sharma AK, Srivastava PC, Johri BN (1994) Contribution of VA mycorrhiza to zinc uptake in plants. In: Manthey JA, Crowley DE, Luster DG (eds) Biochemistry of metal micronutrients in the rhizosphere. Lewis Publishers, Boca Raton, pp 111–123Google Scholar
  112. Sillanpää M (1990) Micronutrient assessment at the country level: an international study. FAO, RomeGoogle Scholar
  113. Singh BK, Nunan N, Ridgway KP et al (2008) Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environ Microbiol 10:534–541.  https://doi.org/10.1111/j.1462-2920.2007.01474.x CrossRefPubMedGoogle Scholar
  114. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  115. Storer K, Coggan A, Ineson P, Hodge A (2017) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 1:1.  https://doi.org/10.1111/nph.14931 CrossRefGoogle Scholar
  116. Stutter MI, Shand CA, George TS et al (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978.  https://doi.org/10.1021/es2044745 CrossRefPubMedGoogle Scholar
  117. Syers JK, John K, Johnston AE, Curtin D (2008) Efficiency of soil and fertilizer phosphorus use. FAO Fertil Plant Nutr Bull 18(108):0259–2495Google Scholar
  118. 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.  https://doi.org/10.1111/j.1365-3040.2005.01360.x CrossRefGoogle Scholar
  119. Tarraf W, Ruta C, Tagarelli A et al (2017) Influence of arbuscular mycorrhizae on plant growth, essential oil production and phosphorus uptake of Salvia officinalis L. Ind Crops Prod 102:144–153.  https://doi.org/10.1016/J.INDCROP.2017.03.010 CrossRefGoogle Scholar
  120. Toler HD, Morton JB, Cumming JR (2005) Growth and metal accumulation of mycorrhizal sorghum exposed to elevated copper and zinc. Water Air Soil Pollut 164:155–172.  https://doi.org/10.1007/s11270-005-2718-z CrossRefGoogle Scholar
  121. Toljander JF, Artursson V, Paul LR et al (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254:34–40.  https://doi.org/10.1111/j.1574-6968.2005.00003.x CrossRefPubMedGoogle Scholar
  122. Turnau K, Kottke I, Oberwinkler F (1993) Element localization in mycorrhizal roots of Pteridium aquilinum (L.) Kuhn collected from experimental plots treated with cadmium dust. New Phytol 123:313–324CrossRefGoogle Scholar
  123. van der Heijden MGA (2010) Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91:1163–1171.  https://doi.org/10.1890/09-0336.1 CrossRefPubMedGoogle Scholar
  124. van der Heijden MGA, Klironomos JN, Ursic M et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.  https://doi.org/10.1038/23932 CrossRefGoogle Scholar
  125. van der Heijden MGA, Streitwolf-Engel R, Riedl R et al (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752.  https://doi.org/10.1111/j.1469-8137.2006.01862.x CrossRefPubMedGoogle Scholar
  126. Van Vuuren DP, Bouwman AF, Beusen AHW (2010) Phosphorus demand for the 1970–2100 period: a scenario analysis of resource depletion. Glob Environ Change 20:428–439.  https://doi.org/10.1016/J.GLOENVCHA.2010.04.004 CrossRefGoogle Scholar
  127. 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.  https://doi.org/10.1111/j.1365-2745.2011.01863.x CrossRefGoogle Scholar
  128. Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62.  https://doi.org/10.1016/J.SOILBIO.2011.11.018 CrossRefGoogle Scholar
  129. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562.  https://doi.org/10.1111/j.1469-8137.2006.01854.x CrossRefPubMedGoogle Scholar
  130. Walley FL, Germida JJ (1997a) Response of spring wheat (Triticum aestivum) to interactions between Pseudomonas species and Glomus clarum NT4. Biol Fertil Soils 24:365–371.  https://doi.org/10.1007/s003740050259 CrossRefGoogle Scholar
  131. Walley FL, Germida JJ (1997b) Response of spring wheat (Triticum aestivum) to interactions between Pseudomonas species and Glomus clarum NT4. Biol Fertil Soils 24:365–371.  https://doi.org/10.1007/s003740050259 CrossRefGoogle Scholar
  132. Watts-Williams SJ, Cavagnaro TR (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294.  https://doi.org/10.1007/s00374-011-0621-x CrossRefGoogle Scholar
  133. Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312.  https://doi.org/10.1007/s11104-013-1670-8 CrossRefGoogle Scholar
  134. White JA, Brown MF (1979) Ultrastructure and X-ray analysis of phosphorus granules in a vesicular–arbuscular mycorrhizal fungus. Can J Bot 57:2812–2818.  https://doi.org/10.1139/b79-333 CrossRefGoogle Scholar
  135. Whiteside MD, Treseder KK, Atsatt PR (2009) The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. Ecology 90:100–108.  https://doi.org/10.1890/07-2115.1 CrossRefPubMedGoogle Scholar
  136. Whiteside MD, Garcia MO, Treseder KK (2012) Amino Acid uptake in arbuscular mycorrhizal plants. PLoS One 7:e47643.  https://doi.org/10.1371/journal.pone.0047643 CrossRefPubMedPubMedCentralGoogle Scholar
  137. Wilson GWT, Hartnett DC (1997) Effects of mycorrhizae on plant growth and dynamics in experimental tallgrass prairie microcosms. Am J Bot 84:478.  https://doi.org/10.2307/2446024 CrossRefPubMedGoogle Scholar
  138. Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738CrossRefPubMedGoogle Scholar
  139. Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392.  https://doi.org/10.1007/s10534-006-9076-1 CrossRefPubMedGoogle Scholar
  140. Wu F, Dong M, Liu Y et al (2011) Effects of long-term fertilization on AM fungal community structure and glomalin-related soil protein in the Loess Plateau of China. Plant Soil 342:233–247.  https://doi.org/10.1007/s11104-010-0688-4 CrossRefGoogle Scholar
  141. Zavalloni C, Vicca S, Büscher M et al (2012) Exposure to warming and CO2 enrichment promotes greater above-ground biomass, nitrogen, phosphorus and arbuscular mycorrhizal colonization in newly established grasslands. Plant Soil 359:121–136.  https://doi.org/10.1007/s11104-012-1190-y CrossRefGoogle Scholar
  142. Zhang X, Chen B, Ohtomo R (2015) Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among different AM fungal species. J Soil Sci Plant Nutr 61:359–368.  https://doi.org/10.1080/00380768.2014.985578 CrossRefGoogle Scholar
  143. Zhu Y-G, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255.  https://doi.org/10.1023/A:1013343811110 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS)AlmoraIndia
  2. 2.Department of Soil Science and Agricultural Chemistry, Institute of Agricultural SciencesBanaras Hindu University (BHU)VaranasiIndia
  3. 3.Department of Agronomy, Institute of Agricultural SciencesBanaras Hindu University (BHU)VaranasiIndia

Personalised recommendations