Plant and Soil

, Volume 300, Issue 1–2, pp 9–20

Mycorrhizal responses to biochar in soil – concepts and mechanisms

  • Daniel D. Warnock
  • Johannes Lehmann
  • Thomas W. Kuyper
  • Matthias C. Rillig
Marschner Review

Abstract

Experiments suggest that biomass-derived black carbon (biochar) affects microbial populations and soil biogeochemistry. Both biochar and mycorrhizal associations, ubiquitous symbioses in terrestrial ecosystems, are potentially important in various ecosystem services provided by soils, contributing to sustainable plant production, ecosystem restoration, and soil carbon sequestration and hence mitigation of global climate change. As both biochar and mycorrhizal associations are subject to management, understanding and exploiting interactions between them could be advantageous. Here we focus on biochar effects on mycorrhizal associations. After reviewing the experimental evidence for such effects, we critically examine hypotheses pertaining to four mechanisms by which biochar could influence mycorrhizal abundance and/or functioning. These mechanisms are (in decreasing order of currently available evidence supporting them): (a) alteration of soil physico-chemical properties; (b) indirect effects on mycorrhizae through effects on other soil microbes; (c) plant–fungus signaling interference and detoxification of allelochemicals on biochar; and (d) provision of refugia from fungal grazers. We provide a roadmap for research aimed at testing these mechanistic hypotheses.

Keywords

Biochar Arbuscular mycorrhiza Ectomycorrhiza Carbon storage Restoration Terra preta 

References

  1. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Angelini J, Castro S, Fabra A (2003) Alterations in root colonization and nodC gene induction in the peanut-rhizobia interaction under acidic conditions. Plant Physiol Biochem 41:289–294CrossRefGoogle Scholar
  3. Antal MJ Jr, Grønli M (2003) The art, science, and technology of charcoal production. Indust Engin Chem Res 42:1619–1640CrossRefGoogle Scholar
  4. Aspray TJ, Eirian Jones E, Whipps JM, Bending GD (2006) Importance of mycorrhization helper bacteria cell density and metabolite localization for the Pinus sylvestris–Lactarius rufus symbiosis. FEMS Microbiol Ecol 56:25–33PubMedCrossRefGoogle Scholar
  5. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32PubMedCrossRefGoogle Scholar
  6. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266PubMedCrossRefGoogle Scholar
  7. Baldock JA, Smernik RJ (2002) Chemical composition and bioavailability of thermally altered Pinus resinosa (Red pine) wood. Organic Geochem 33:1093–1109CrossRefGoogle Scholar
  8. Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular–arbuscular mycorrhizal symbiosis. Appl Environ Microb 55:2320–2325Google Scholar
  9. Cohn J, Bradley D, Stacey G (1998) Legume nodule organogenesis. Trends Plant Sci 3:105–110CrossRefGoogle Scholar
  10. Day D, Evans RJ, Lee JW, Reicosky D (2005) Economical CO2, SOx, and NOx capture from fossil-fuel utilization with combined renewable hydrogen production and large-scale carbon sequestration. Energy 30:2558–2579CrossRefGoogle Scholar
  11. DeLuca TH, MacKenzie MD, Gundale MJ, Holben WE (2006) Wildfire-produced charcoal directly influences nitrogen cycling in ponderosa pine forests. Soil Sci Soc Am J 70:448–453CrossRefGoogle Scholar
  12. Drew EA, Murray RS, Smith SE (2006) Functional diversity of external hyphae of AM fungi: ability to colonize new hosts is influenced by fungal species, distance and soil conditions. Appl Soil Ecol 32:350–365CrossRefGoogle Scholar
  13. Duclos JL, Fortin JA (1983) Effect of glucose and active charcoal on in-vitro synthesis of ericoid mycorrhiza with Vaccinium spp. New Phytol 94:95–102CrossRefGoogle Scholar
  14. Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13:85–91PubMedCrossRefGoogle Scholar
  15. Escudero V, Mendoza RE (2005) Seasonal variation of arbuscular mycorrhizal fungi in temperate grasslands along a wide hydrologic gradient. Mycorrhiza 15:291–299PubMedCrossRefGoogle Scholar
  16. Ezawa T, Yamamoto K, Yoshida S (2002) Enhancement of the effectiveness of indigenous arbuscular mycorrhizal fungi by inorganic soil amendments. Soil Sci Plant Nutr 48:897–900Google Scholar
  17. Founoune H, Duponnois R, Bâ AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL (2002) Mycorrhiza Helper Bacteria stimulate ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus. New Phytol 153:81–89CrossRefGoogle Scholar
  18. Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  19. Gaur A, Adholeya A (2000) Effects of the particle size of soil-less substrates upon AM fungus inoculum production. Mycorrhiza 10:43–48CrossRefGoogle Scholar
  20. Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular–arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255Google Scholar
  21. Glaser B (2007) Prehistorically modified soils of central Amazonia: a model for sustainable agriculture in the twenty-first century. Phil Trans R Soc B 362:187–196PubMedCrossRefGoogle Scholar
  22. Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal – a review. Biol Fert Soils 35:219–230CrossRefGoogle Scholar
  23. Glaser B, Woods W (2004) Towards an understanding of amazon dark earths. In: B Glaser, W Woods (eds)Amazon dark earths: explorations in space and time. Springer, Berlin, pp 1–8Google Scholar
  24. Gundale MJ, DeLuca TH (2006) Temperature and source material influence ecological attributes of Ponderosa pine and Douglas-fir charcoal. For Ecol Manag 231:86–93CrossRefGoogle Scholar
  25. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefGoogle Scholar
  26. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 135:335–344CrossRefGoogle Scholar
  27. Harvey AE, Jurgensen MF, Larsen MJ (1976) Comparative distribution of ectomycorrhizae in a mature Douglas-fir/Larch forest soil in western Montana. Forest Sci 22:350–358Google Scholar
  28. Harvey AE, Jurgensen MF, Larsen MJ (1978) Seasonal distribution in a mature Douglas-fir/Larch forest soil in western Montana. Forest Sci 22:203–208Google Scholar
  29. Harvey AE, Larsen MF, Jurgensen MF (1979) Comparative distribution of ectomycorrhizae in soils of three western Montana forest habitat types. Forest Sci 25:350–358Google Scholar
  30. Herrmann S, Oelmuller R, Buscot F (2004) Manipulation of the onset of ectomycorrhiza formation by indole-3-acetic acid, activated charcoal or relative humidity in the association between oak micro-cuttings and Piloderma croceum: influence on plant development and photosynthesis. J Plant Physiol 161:509–517PubMedCrossRefGoogle Scholar
  31. Hildebrandt U, Janetta, K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microb 68:1919–1924CrossRefGoogle Scholar
  32. Hildebrandt U, Ouziad F, Marner F-J, Bothe H (2006) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett 254:258–267PubMedCrossRefGoogle Scholar
  33. Hockaday WC, Grannas AM, Kim S, Hatcher PG (2007) The transformation and mobility of charcoal in a fire-impacted watershed. Geochim Cosmochim Ac 71:3432–3445CrossRefGoogle Scholar
  34. Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678PubMedCrossRefGoogle Scholar
  35. Ishii T, Kadoya K (1994) Effects of charcoal as a soil conditioner on citrus growth and vesicular–arbuscular mycorrhizal development. J Jpn Soc Hortic Sci 63:529–535Google Scholar
  36. Johnson NC, Tilman D, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042CrossRefGoogle Scholar
  37. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae?. Ecol Appl 3:749–757CrossRefGoogle Scholar
  38. Kawamoto K, Ishimaru K, Imamura Y (2005) Reactivity of wood charcoal with ozone. Wood Sci 51:66–72CrossRefGoogle Scholar
  39. Keech O, Carcaillet C, Nilsson MC (2005) Adsorption of allelopathic compounds by wood-derived charcoal: the role of wood porosity. Plant Soil 272:291–300CrossRefGoogle Scholar
  40. Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fert Soils 21:43–52CrossRefGoogle Scholar
  41. Knicker H (2007) How does fire affect the nature and stability of soil organic nitrogen and carbon? A review. Biogeochemistry 85:91–118CrossRefGoogle Scholar
  42. Kothamasi D, Kothamasi S, Bhattacharyya A, Kuhad RC, Babu CR (2006) Arbuscular mycorrhizae and phosphate solubilising bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India. Biol Fert Soils 42:358–361CrossRefGoogle Scholar
  43. Krull ES, Skjemstad JO, Graetz D, Grice K, Dunning W, Cook G, Parr JF (2003) 13C-depleted charcoal from C4 grasses and the role of occluded carbon in phytoliths. Org Geochem 34:1337–1352CrossRefGoogle Scholar
  44. Kwon S, Pignatello JJ (2005) Effect of natural organic substances on the surface and adsorptive properties of environmental black carbon (char): pseudo pore blockage by model lipid components and its implications for N2-probed surface properties of natural sorbents. Env Sci Technol 39:7932–7939CrossRefGoogle Scholar
  45. Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22CrossRefGoogle Scholar
  46. Lehmann J (2007) Bio-energy in the black. Frontiers in Ecology and the Environment 5:381–387CrossRefGoogle Scholar
  47. Lehmann J, Da Silva JP Jr, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil 249:343–357CrossRefGoogle Scholar
  48. Lehmann J, Gaunt J, Rondon M (2006) Biochar sequestration in terrestrial ecosystems – a review. Mitig Adapt Strat Global Change 11:403–427CrossRefGoogle Scholar
  49. Lucas RE, Davis JF (1961) Relationships between pH values of organic soils and availabilities of 12 plant nutrients. Soil Sci 92:177–182CrossRefGoogle Scholar
  50. Major J, Steiner C, Ditommaso A, Falcão NP, Lehmann J (2005) Weed composition and cover after three years of soil fertility management in the central Brazilian Amazon: compost, fertilizer, manure and charcoal applications. Weed Biol Manag 5:69–76CrossRefGoogle Scholar
  51. Marris E (2006) Black is the new green. Nature 442:624–626PubMedCrossRefGoogle Scholar
  52. Matsubara Y-I, Hasegawa N, Fukui H (2002) Incidence of Fusarium root rot in asparagus seedlings infected with arbuscular mycorrhizal fungus as affected by several soil amendments. J Jpn Soc Hortic Sci 71:370–374CrossRefGoogle Scholar
  53. Miller RM, Miller SP, Jastrow JD, Rivetta CB (2002) Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytol 155:149–162CrossRefGoogle Scholar
  54. Mori S, Marjenah (1994) Effect of charcoaled rice husks on the growth of Dipterocarpaceae seedlings in East Kalimantan with special reference to ectomycorrhiza formation. J Jap Forestry Soc 76:462–464Google Scholar
  55. Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90CrossRefGoogle Scholar
  56. Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular–arbuscular mycorrhiza-stimulatory compounds from clover (Trifolium repens) roots. Appl Environ Microb 57:434–439Google Scholar
  57. Oguntunde PG, Fosu M, Ajayi AE, Van De Giesen ND (2004) Effects of charcoal production on maize yield, chemical properties and texture of soil. Biol Fert Soils 39:295–299CrossRefGoogle Scholar
  58. Pan MJ, Van Staden J (1998) The use of charcoal in in-vitro culture – A review. Plant Growth Regul 26:155–163CrossRefGoogle Scholar
  59. Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses. New Phytol 172:35–46PubMedCrossRefGoogle Scholar
  60. Pietikäinen J, Kiikkilä O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 89:231–242CrossRefGoogle Scholar
  61. Preston CM, Schmidt MWI (2006) Black (pyrogenic) carbon: A synthesis of current knowledge and uncertainties with special consideration of boreal regions. Biogeosciences 3:397–420CrossRefGoogle Scholar
  62. Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263CrossRefGoogle Scholar
  63. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler H-P (2006) Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microb 72:3550–3557CrossRefGoogle Scholar
  64. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754CrossRefGoogle Scholar
  65. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53PubMedCrossRefGoogle Scholar
  66. Rondon M, Lehmann J, Ramírez J, Hurtado MP (2007) Biological nitrogen fixation by common beans (Phaseolus vulgaris L.) increases with biochar additions. Biol Fert Soils 43:699–708CrossRefGoogle Scholar
  67. Saito M (1990) Charcoal as a micro habitat for VA mycorrhizal fungi, and its practical application. Agric Ecosyst Environ 29:341–344CrossRefGoogle Scholar
  68. Samonin VV, Elikova EE (2004) A study of the adsorption of bacterial cells on porous materials. Microbiology 73:810–816PubMedCrossRefGoogle Scholar
  69. Schiermeier Q (2006) Putting the carbon back. Nature 442:620–623PubMedCrossRefGoogle Scholar
  70. Schmidt MWI, Noack AG (2000) Black carbon in soils and sediments: Analysis, distribution, implications and current challenges. Global Biogeochem Cy 14:777–793CrossRefGoogle Scholar
  71. Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515PubMedCrossRefGoogle Scholar
  72. Skjemstad JO, Janik LJ, Taylor JA (1998) Non-living soil organic matter: What do we know about it? Aust. J Exp Agr 38:667–680CrossRefGoogle Scholar
  73. Swift RS (2001) Sequestration of carbon by soil. Soil Sci 166:858–871CrossRefGoogle Scholar
  74. Swift MJ, Heal OW, Anderson JW (1979) Decomposition in terrestrial ecosystems. University of California Press, BerkeleyGoogle Scholar
  75. Topoliantz S, Ponge J-F, Ballof S (2005) Manioc peel and charcoal: a potential organic amendment for sustainable soil fertility in the tropics. Biol Fert Soils 41:15–21CrossRefGoogle Scholar
  76. Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515CrossRefGoogle Scholar
  77. Tryon EH (1948) Effect of charcoal on certain physical, chemical, and biological properties of forest soils. Ecol Monogr 18:81–115CrossRefGoogle Scholar
  78. Vaario LM, Tanaka M, Ide Y, Gill WM, Suzuki K (1999) In vitro ectomycorrhiza formation between Abies firma and Pisolithus tinctorius. Mycorrhiza 9:177–183CrossRefGoogle Scholar
  79. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095PubMedCrossRefGoogle Scholar
  80. Van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  81. Wallstedt A, Coughlan A, Munson AD, Nilsson MC, Margolis HA (2002) Mechanisms of interaction between Kalmia angustifolia cover and Picea mariana seedlings. Can J For Res 32:2022–2031CrossRefGoogle Scholar
  82. Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525PubMedGoogle Scholar
  83. Yamato M, Okimori Y, Wibowo IF, Anshiori S, Ogawa M (2006) Effects of the application of charred bark of Acacia mangium on the yield of maize, cowpea and peanut, and soil chemical properties in South Sumatra, Indonesia. Soil Sci Plant Nutr 52:489–495CrossRefGoogle Scholar
  84. Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil–plant systems. Trends Plant Sci 8:407–409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Daniel D. Warnock
    • 1
  • Johannes Lehmann
    • 2
  • Thomas W. Kuyper
    • 3
  • Matthias C. Rillig
    • 1
    • 4
  1. 1.Microbial Ecology Program, Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Department of Crop and Soil SciencesCornell UniversityIthacaUSA
  3. 3.Department of Soil QualityWageningen UniversityWageningenThe Netherlands
  4. 4.Institut für BiologieFreie Universität BerlinBerlinGermany

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