Plant and Soil

, Volume 395, Issue 1–2, pp 105–123

Phosphorus availability to beans via interactions between mycorrhizas and biochar

Regular Article
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Abstract

Background and aims

We sought to understand biochar’s role in promoting plant phosphorus (P) access via arbuscular mycorrhizas (AM), focusing on whether P solubility and biochar-P proximity altered AM enhancement of P uptake in a mycorrhizal crop legume.

Methods

A greenhouse study compared feedstock-derived P with 50 mg P pot−1 of sparingly soluble FePO4 (Fe-P) or soluble NaH2PO4 (Na-P) at different proximities to biochar (co-pyrolyzed, mixed with biochar, mixed with soil) on Phaseolus vulgaris P uptake, specific root length (SRL), AM colonization, AM neutral lipids, and microbial biomass-P.

Results

Biochar increased AM colonization by 6 % (p < 0.01) and increased Fe-P uptake from 3.1 to 3.8 mg plant−1, with AM-related Fe-P uptake increased by 12 % (p < 0.05). Regardless of proximity, biochar applied with Fe-P was enriched (>2×) with AM hyphae. Biochar-P proximity did not alter P uptake, but shifted uptake towards AM for Fe-P and roots for Na-P. Soluble P located on biochar increased total plant + microbial P (p < 0.05). Biochar reversed (p < 0.05) reductions in SRL induced by AM.

Conclusions

Biochar enhanced AM’s access to sparingly soluble P, and root/microbial access to soluble P. Biochar augments sparingly soluble P uptake at scales larger than biochar particles, perhaps by reducing P sorption or facilitating root/hyphal exploration.

Keywords

Biochar Iron phosphate Microbial biomass Mycorrhizas Phaseolus vulgaris Phosphorus fixation NLFA Rhizosphere 

Supplementary material

11104_2014_2246_MOESM1_ESM.docx (2.4 mb)
ESM 1(DOCX 2.36 mb)

References

  1. Ahmad F, Tan KH (1991) Availability of fixed phosphate to corn (zea mays l.) seedlings as affected by humic acids. Indones J Trop Agric 2:66–72Google Scholar
  2. Ahmed FRS, Alexander IJ, Mwinyihija M, Killham K (2011) Effect of superphosphate and arbuscular mycorrhizal fungus Glomus mosseae on phosphorus and arsenic uptake in lentil (Lens culinaris L.). Water Air Soil Pollut 221:169–182CrossRefGoogle Scholar
  3. Alameda D, Villar R (2012) Linking root traits to plant physiology and growth in Fraxinus angustifolia Vahl. seedlings under soil compaction conditions. Environ Exp Bot 79:49–57CrossRefGoogle Scholar
  4. Alguacil MD, Roldan A, Salinas-Garcia JR, Querejeta JI (2011) No tillage affects the phosphorus status, isotopic composition and crop yield of Phaseolus vulgaris in a rain-fed farming system. J Sci Food Agr 91:268–272CrossRefGoogle Scholar
  5. Ameloot N, De Neve S, Jegajeevagan K, Yildiz G, Buchan D, Funkuin YN, Prins W, Bouckaert L, Sleutel S (2013) Short-term CO2 and N2O emissions and microbial properties of biochar amended sandy loam soils. Soil Biol Biochem 57:401–410CrossRefGoogle Scholar
  6. Amonette JE, Joseph SD (2009) Characteristics of biochar: micro-chemical properties. In: Lehmann J, Joseph SD (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 35–52Google Scholar
  7. Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: A review. Plant Soil 337:1–18CrossRefGoogle Scholar
  8. Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: A review. J Soil Sci Plant Nutr 12:547–561CrossRefGoogle Scholar
  9. Belyaeva ON, Haynes RJ (2012) Comparison of the effects of conventional organic amendments and biochar on the chemical, physical and microbial properties of coal fly ash as a plant growth medium. Env Earth Sci 66:1987–1997CrossRefGoogle Scholar
  10. Borggaard OK, Raben-Lange B, Gimsing AL, Strobel BW (2005) Influence of humic substances on phosphate adsorption by aluminium and iron oxides. Geoderma 127:270–279CrossRefGoogle Scholar
  11. Bossio D, Scow K, Gunapala N, Graham K (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12CrossRefPubMedGoogle Scholar
  12. Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329CrossRefGoogle Scholar
  13. Case SDC, McNamara NP, Reay DS, Whitaker J (2012) The effect of biochar addition on N2O and CO2 emissions from a sandy loam soil - the role of soil aeration. Soil Biol Biochem 51:125–134CrossRefGoogle Scholar
  14. Chacon N, Silver WL, Dubinsky EA, Cusack DF (2006) Iron reduction and soil phosphorus solubilization in humid tropical forests soils: the roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67–84CrossRefGoogle Scholar
  15. Chakraborty D, Garg RN, Tomar RK, Dwivedi BS, Aggarwal P, Singh R, Behera UK, Thangasamy A, Singh D (2010) Soil physical quality as influenced by long-term application of fertilizers and manure under maize-wheat system. Soil Sci 175:128–136CrossRefGoogle Scholar
  16. Cui M, Caldwell MM (1996) Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches.1. Roots and hyphae exploiting the same soil volume. New Phytol 133:453–460CrossRefGoogle Scholar
  17. Cui HJ, Wang MK, Fu ML, Ci E (2011) Enhancing phosphorus availability in phosphorus-fertilized zones by reducing phosphate adsorbed on ferrihydrite using rice straw-derived biochar. J Soils Sediments 11:1135–1141CrossRefGoogle Scholar
  18. Deenik JL, Diarra A, Uehara G, Campbell S, Sumiyoshi Y, Antal MJ (2011) Charcoal ash and volatile matter effects on soil properties and plant growth in an acid ultisol. Soil Sci 176:336–345CrossRefGoogle Scholar
  19. Dempster DN, Gleeson DB, Solaiman ZM, Jones DL, Murphy DV (2012) Decreased soil microbial biomass and nitrogen mineralisation with eucalyptus biochar addition to a coarse textured soil. Plant Soil 354:311–324CrossRefGoogle Scholar
  20. Elmer WH, Pignatello JJ (2011) Effect of biochar amendments on mycorrhizal associations and fusarium crown and root rot of asparagus in replant soils. Plant Dis 95:960–966CrossRefGoogle Scholar
  21. Enders A, Lehmann J (2012) Comparison of wet-digestion and dry-ashing methods for total elemental analysis of biochar. Commun Soil Sci Plan 43:1042–1052CrossRefGoogle Scholar
  22. Erich MS, Fitzgerald CB, Porter GA (2002) The effect of organic amendments on phosphorus chemistry in a potato cropping system. Agr Ecosyst Environ 88:79–88CrossRefGoogle Scholar
  23. Gerke J (2010) Humic (organic matter)-Al(Fe)-phosphate complexes: an underestimated phosphate form in soils and source of plant-available phosphate. Soil Sci 175:417–425CrossRefGoogle Scholar
  24. Gichangi EM, Mnkeni PNS, Brookes PC (2010) Goat manure application improves phosphate fertilizer effectiveness through enhanced biological cycling of phosphorus. Soil Sci Plant Nutr 56:853–860CrossRefGoogle Scholar
  25. Gollner MJ, Wagentristl H, Liebhard P, Friedel JK (2011) Yield and arbuscular mycorrhiza of winter rye in a 40-years fertilisation trial. Agron Sustain Dev 31:373–378CrossRefGoogle Scholar
  26. Gregorich EG, Wen G, Voroney RP, Kachanoski RG (1990) Calibration of a rapid direct chloroform extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 22:1009–1011CrossRefGoogle Scholar
  27. Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80:695–720CrossRefGoogle Scholar
  28. Guppy CN, Menzies NW, Moody PW, Blamey FPC (2005) Competitive sorption reactions between phosphorus and organic matter in soil: a review. Aust J Soil Res 43:189–202CrossRefGoogle Scholar
  29. Haynes RJ, Mokolobate MS (2001) Amelioration of al toxicity and p deficiency in acid soils by additions of organic residues: a critical review of the phenomenon and the mechanisms involved. Nutr Cycl Agroecosyst 59:47–63CrossRefGoogle Scholar
  30. Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362CrossRefGoogle Scholar
  31. Hetrick BAD, Wilson GWT, Todd TC (1992) Relationships of mycorrhizal symbiosis, rooting strategy, and phenology among tallgrass prairie forbs. Can J Bot 70:1521–1528CrossRefGoogle Scholar
  32. Hue NV (1991) Effects of organic-acids anions on p-sorption and phytoavailability in soils with different mineralogies. Soil Sci 152:463–471CrossRefGoogle Scholar
  33. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647CrossRefPubMedGoogle Scholar
  34. Joseph SD, Camps-Arbestain M, Lin Y, Munroe P, Chia CH, Hook J, van Zwieten L, Kimber S, Cowie A, Singh BP, Lehmann J, Foidl N, Smernik RJ, Amonette JE (2010) An investigation into the reactions of biochar in soil. Aust J Soil Res 48:501–515CrossRefGoogle Scholar
  35. Kalra YP (1998) Handbook of reference methods for plant analysis. CRC Press, Boca RatonGoogle Scholar
  36. Kimetu JM, Lehmann J, Ngoze SO, Mugendi DN, Kinyangi JM, Riha S, Verchot L, Recha JW, Pell AN (2008) Reversibility of soil productivity decline with organic matter of differing quality along a degradation gradient. Ecosystems 11:726–739CrossRefGoogle Scholar
  37. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect va mycorrhizas. Mycol Res 92:486–488CrossRefGoogle Scholar
  38. Kudeyarova AY (2010) Chemisorption of phosphate ions and destruction of organomineral sorbents in acid soils. Eurasian Soil Sci 43:635–650CrossRefGoogle Scholar
  39. Kuzyakov Y, Bogomolova I, Glaser B (2014) Biochar stability in soil: decomposition during 8 years and transformation as assessed by compound-specific 14c analysis. Soil Biol Biochem 70:229–236CrossRefGoogle Scholar
  40. Larsen J, Olsson PA, Jakobsen I (1998) The use of fatty acid signatures to study mycelial interactions between the arbuscular mycorrhizal fungus Glomus intraradices and the saprotrophic fungus Fusarium culmorum in root-free soil. Mycol Res 102:1491–1496CrossRefGoogle Scholar
  41. LeCroy C, Masiello CA, Rudgers JA, Hockaday WC, Silberg JJ (2013) Nitrogen, biochar, and mycorrhizae: alteration of the symbiosis and oxidation of the char surface. Soil Biol Biochem 58:248–254CrossRefGoogle Scholar
  42. Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota – a review. Soil Biol Biochem 43:1812–1836CrossRefGoogle Scholar
  43. Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units–adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345CrossRefPubMedGoogle Scholar
  44. Lineweaver H, Burk D (1934) The determination of enzyme dissociation constants. J Am Chem Soc 56(3):658–666. doi:10.1021/ja01318a036 CrossRefGoogle Scholar
  45. Lobartini JC, Tan KH, Pape C (1998) Dissolution of aluminum and iron phosphate by humic acids. Commun Soil Sci Plan 29:535–544CrossRefGoogle Scholar
  46. Lynch J, Brown KM (1997) Ethylene and plant responses to nutritional stress. Physiol Plant 100:613–619CrossRefGoogle Scholar
  47. Miyauchi MYH, Lima DS, Nogueira MA, Lovato GM, Murate LS, Cruz MF, Ferreira JM, Zangaro W, Andrade G (2008) Interactions between diazotrophic bacteria and mycorrhizal fungus in maize genotypes. Sci Agric 65:525–531CrossRefGoogle Scholar
  48. Morales MM, Comerford N, Guerrini IA, Falcão NPS, Reeves JB (2013) Sorption and desorption of phosphate on biochar and biochar-soil mixtures. Soil Use Manag 29:306–314CrossRefGoogle Scholar
  49. Mukherjee A, Zimmerman AR (2013) Organic carbon and nutrient release from a range of laboratory-produced biochars and biochar–soil mixtures. Geoderma 193–194:122–130CrossRefGoogle Scholar
  50. Nzanza B, Marais D, Soundy P (2012) Effect of arbuscular mycorrhizal fungal inoculation and biochar amendment on growth and yield of tomato. Int J Agric Biol 14:965–969Google Scholar
  51. Ostonen I, Puttsepp U, Biel C, Alberton O, Bakker MR, Lohmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442CrossRefGoogle Scholar
  52. Pang JY, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255CrossRefGoogle Scholar
  53. Quilliam RS, Marsden KA, Gertler C, Rousk J, DeLuca TH, Jones DL (2012a) Nutrient dynamics, microbial growth and weed emergence in biochar amended soil are influenced by time since application and reapplication rate. Agric Ecosyst Environ 158:192–199CrossRefGoogle Scholar
  54. Quilliam RS, DeLuca TH, Jones DL (2012b) Biochar application reduces nodulation but increases nitrogenase activity in clover. Plant Soil 366:83–92CrossRefGoogle Scholar
  55. Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156CrossRefGoogle Scholar
  56. Richter DD, Markewitz D, Wells CG, Allen HL, April R, Heine PR, Urrego B (1994) Soil chemical-change during 3 decades in an old-field loblolly-pine (Pinus-taeda L.) ecosystem. Ecology 75:1463–1473CrossRefGoogle Scholar
  57. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to IMAGE-J: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMedGoogle Scholar
  58. Schnoor TK, Martensson LM, Olsson PA (2011) Soil disturbance alters plant community composition and decreases mycorrhizal carbon allocation in a sandy grassland. Oecologia 167:809–819CrossRefPubMedGoogle Scholar
  59. Schomberg HH, Gaskin JW, Harris K, Das KC, Novak JM, Busscher WJ, Watts DW, Woodroof RH, Lima IM, Ahmedna M, Rehrah D, Xing BS (2012) Influence of biochar on nitrogen fractions in a coastal plain soil. J Environ Qual 41:1087–1095CrossRefPubMedGoogle Scholar
  60. Seguel A, Cumming JR, Klugh-Stewart K, Cornejo P, Borie F (2013) The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: a review. Mycorrhiza 23:167–183CrossRefPubMedGoogle Scholar
  61. Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2009) Influence of arbuscular mycorrhizae on the root system of maize plants under salt stress. Can J of Microbiol 55:879–886CrossRefGoogle Scholar
  62. Shi Z, Wang F, Zhang C, Yang Z (2011) Exploitation of phosphorus patches with different phosphorus enrichment by three arbuscular mycorrhizal fungi. J Plant Nutr 34:1096–1106CrossRefGoogle Scholar
  63. Silva GL, Lima HV, Campanha MM, Gilkes RJ, Oliveira TS (2011) Soil physical quality of luvisols under agroforestry, natural vegetation and conventional crop management systems in the Brazilian semi-arid region. Geoderma 167–68:61–70CrossRefGoogle Scholar
  64. Simojoki A (2001) Morphological responses of barley roots to soil compaction and modified supply of oxygen. Agr Food Sci Finl 10:45–52Google Scholar
  65. Snapp S, Koide R, Lynch J (1995) Exploitation of localized phosphorus-patches by common bean roots. Plant Soil 177:211–218CrossRefGoogle Scholar
  66. Spokas KA, Baker JM, Reicosky DC (2010) Ethylene: potential key for biochar amendment impacts. Plant Soil 333:443–452CrossRefGoogle Scholar
  67. Useche A, Shipley B (2010) Plasticity in relative growth rate after a reduction in nitrogen availability is related to root morphological and physiological responses. Ann Bot-Lond 106:617–625CrossRefGoogle Scholar
  68. Van Aarle IM, Olsson PA (2003) Fungal lipid accumulation and development of mycelial structures by two arbuscular mycorrhizal fungi. Appl Environ Microbiol 69:6762–6767PubMedCentralCrossRefPubMedGoogle Scholar
  69. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397PubMedCentralCrossRefPubMedGoogle Scholar
  70. Warnock DD, Lehmann J, Kuyper TW, Rillig MC (2007) Mycorrhizal responses to biochar in soil – concepts and mechanisms. Plant Soil 300:9–20CrossRefGoogle Scholar
  71. Warnock DD, Mummey DL, McBride B, Major J, Lehmann J, Rillig MC (2010) Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal abundances in roots and soils: Results from growth-chamber and field experiments. Appl Soil Ecol 46:450–456CrossRefGoogle Scholar
  72. Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S (2010) Sustainable biochar to mitigate global climate change. Nat Comm 1:56. doi:10.1038/ncomms1053 CrossRefGoogle Scholar
  73. Xu G, Wei LL, Sun JN, Shao HB, Chang SX (2013) What is more important for enhancing nutrient bioavailability with biochar application into a sandy soil: direct or indirect mechanism? Ecol Eng 52:119–124CrossRefGoogle Scholar
  74. Yan XL, Lynch JP, Beebe SE (1996) Utilization of phosphorus substrates by contrasting common bean genotypes. Crop Sci 36:936–941CrossRefGoogle Scholar
  75. Zaifnejad M, Clark RB, Sullivan CY (1997) Aluminum and water stress effects on growth and proline of sorghum. J Plant Physiol 150:338–344CrossRefGoogle Scholar
  76. Zimmerman AR (2010) Abiotic and microbial oxidation of laboratory-produced black carbon (biochar). Environ Sci Technol 44:1295–1301CrossRefPubMedGoogle Scholar
  77. Zobel RW, Alloush GA, Belesky DP (2006) Differential root morphology response to no versus high phosphorus, in three hydroponically grown forage chicory cultivars. Environ Exp Bot 57:201–208CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of GeographyPenn State UniversityState CollegeUSA
  2. 2.Department of Crop and Soil SciencesCornell UniversityIthacaUSA

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