Biology and Fertility of Soils

, Volume 54, Issue 8, pp 935–947 | Cite as

Urochloa ruziziensis cover crop increases the cycling of soil inositol phosphates

  • Danilo S. AlmeidaEmail author
  • Daniel Menezes-Blackburn
  • Benjamin L. Turner
  • Catherine Wearing
  • Philip M. Haygarth
  • Ciro A. Rosolem
Original Paper


Ruzigrass (Urochloa ruziziensis) is a cover crop that is commonly used in Brazil and exudes high concentrations of organic acids from its roots, and is therefore expected to mobilize soil organic P such as inositol phosphates. However, it is not known if this can occur only under P deficient conditions. Specifically, we aimed to test the hypothesis that the degradation of inositol phosphates is increased by growing ruzigrass at two different P levels. To investigate this, we studied soil organic P in a 9-year-old field experiment, with treatments consisting of ruzigrass or fallow during the soybean (Glycine max) off-season, with or without P addition. Organic P was extracted in NaOH-EDTA, followed by colorimetric quantification of organic P hydrolysable by phytase, and myo-inositol hexakisphosphate by hypobromite oxidation and HPLC separation. Ruzigrass dry matter yield increased by about 80% with P application. Ruzigrass reduced the concentration of phytase labile P and myo-inositol hexakisphosphate, but only in soil receiving P. A corresponding increase in unidentified inositol phosphates, presumably representing lower-order esters, was also observed after ruzigrass in soil with P application. We deduce that the degradation of inositol phosphates under ruzigrass with P application is due to greater ruzigrass productivity in the more fertile treatment, increasing the release of root exudates that solubilize inositol phosphates and promote their decomposition by phytase. We conclude that ruzigrass cover cropping can promote the cycling of recalcitrant soil organic P, but only when fertility is raised to a sufficient level to ensure a productive crop.


myo-Inositol hexakisphosphate Organic phosphorus No-till Cover crops Hypobromite oxidation 


Funding information

This research was supported by São Paulo Research Foundation (FAPESP) grants #2014/23707-5 and #2015/04200-0. This work was performed as part of the Organic Phosphorus Utilisation in Soils (OPUS) project, funded by Biotechnology and Biological Sciences Research Council (BBSRC) responsive mode grant (BB/K018167/1) in the UK to explore cropping strategies to target the use of recalcitrant soil organic phosphorus. We would also like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for granting a scholarship to the first author.


  1. Almeida DS, Rosolem CA (2016) Ruzigrass grown in rotation with soybean increases soil labile phosphorus. Agron J 108:1–9. CrossRefGoogle Scholar
  2. Alvear M, Rosas A, Rouanet JL, Borie F (2005) Effects of three soil tillage systems on some biological activities in an Ultisol from southern Chile. Soil Tillage Res 82:195–202. CrossRefGoogle Scholar
  3. Appelhans SC, Melchiori RJ, Barbagelata PA, Novelli LE (2016) Assessing organic phosphorus contributions for predicting soybean response to fertilization. Soil Sci Soc Am J 80:1688–1697. CrossRefGoogle Scholar
  4. Awan AB (1964) Influence of mulch on soil moisture, soil temperature and yield of potatoes. Am Potato J 41:337–339. CrossRefGoogle Scholar
  5. Begum HH, Osaki M, Nanamori M, Watanabe T, Shinano T, Rao IM (2006) Role of phosphoenolpyruvate carboxylase in the adaptation of a tropical forage grass to low-phosphorus acid soils. J Plant Nutr 29:35–57. CrossRefGoogle Scholar
  6. Bowman RA, Moir JO (1993) Basic EDTA as an extractant for soil organic phosphorus. Soil Sci Soc Am J 57:1516–1518. CrossRefGoogle Scholar
  7. Bünemann EK, Bossio DA, Smithson PC, Frossard E, Oberson A (2004) Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol Biochem 36:889–901. CrossRefGoogle Scholar
  8. Cade-Menun BJ (2017) Characterizing phosphorus forms in cropland soils with solution 31P-NMR: past studies and future research needs. Chem Biol Technol Agric 4:4–19. CrossRefGoogle Scholar
  9. Cade-Menun B, Liu CW (2014) Solution phosphorus-31 nuclear magnetic resonance spectroscopy of soils from 2005 to 2013: a review of sample preparation and experimental parameters. Soil Sci Soc Am J 78:19–37. CrossRefGoogle Scholar
  10. Calegari A, Tiecher T, Hargrove WL, Ralisch R, Tessier D, de Tourdonnet S, Guimarães MF, dos Santos DR (2013) Long-term effect of different soil management systems and winter crops on soil acidity and vertical distribution of nutrients in a Brazilian Oxisol. Soil Tillage Res 133:32–39. CrossRefGoogle Scholar
  11. Celi L, Barberis E (2007) Abiotic reactions of inositol phosphates in soil. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, pp 207–220CrossRefGoogle Scholar
  12. Celi L, Lamacchia S, Marsan FA, Barberis E (1999) Interaction of inositol hexaphosphate on clays: adsorption and charging phenomena. Soil Sci 164:574–585CrossRefGoogle Scholar
  13. Cepagri (2015) Clima dos municípios paulistas: Botucatu Accessed 20 Sep. 2015
  14. Chapuis-Lardy L, Brossard M, Quiquampoix H (2001) Assessing organic phosphorus status of Cerrado Oxisols (Brazil) using 31P-NMR spectroscopy and phosphomonoesterase activity measurement. Can J Soil Sci 81:591–601. CrossRefGoogle Scholar
  15. Condron LM, Turner BL, Cade-Menun BJ (2005) Chemistry and dynamics of soil organic phosphorus. In: Sims JT, Sharpley AN (eds) Phosphorus: agriculture and the environment. Agronomy monograph, vol 46. ASA-CSSA-SSSA, Madison, pp 87–121. CrossRefGoogle Scholar
  16. Costa AR, Sato JH, Ramos MLG, Figueiredo CC, Souza GP, Rocha OC, Guerra AF (2013) Microbiological properties and oxidizable organic carbon fractions of an Oxisol under coffee with split phosphorus applications and irrigation regimes. Rev Bras Cienc Solo 37:55–65. CrossRefGoogle Scholar
  17. Costa SEVGA, Souza ED, Anghinoni I, Carvalho PCF, Martins AP, Kunrath TR, Cecagno D, Balerini F (2014) Impact of an integrated no-till crop–livestock system on phosphorus distribution, availability and stock. Agric Ecosyst Environ 190:43–51. CrossRefGoogle Scholar
  18. Espinosa M, Turner BL, Haygarth PM (1999) Preconcentration and separation of trace phosphorus compounds in soil leachate. J Environ Qual 28:1497–1504. CrossRefGoogle Scholar
  19. Franzluebbers AJ, Sawchik J, Taboada MA (2014) Agronomic and environmental impacts of pasture–crop rotations in temperate North and South America. Agric Ecosyst Environ 190:18–26. CrossRefGoogle Scholar
  20. Gatiboni LC, Santos DR, Claro Flores AF, Anghinoni I, Kaminski J, Lima MS (2005) Phosphorus forms and availability assessed by 31P-NMR in successive cropped soil. Commun Soil Sci Plant Anal 36:2625–2640. CrossRefGoogle Scholar
  21. George TS, Simpson RJ, Hadobas PA, Marshall DJ, Richardson AE (2007) Accumulation and phosphatase-lability of organic phosphorus in fertilised pasture soils. Aust J Agric Res 58:47–55. CrossRefGoogle Scholar
  22. Gerke J (2015) Phytate (inositol hexakisphosphate) in soil and phosphate acquisition from inositol phosphates by higher plants: a review. Plants 4:253–266. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Giaveno C, Celi L, Richardson AE, Simpson RJ, Barberis E (2010) Interaction of phytases with minerals and availability of substrate affect the hydrolysis of inositol phosphates. Soil Biol Biochem 42:491–498. CrossRefGoogle Scholar
  24. Harrison AF (1987) Soil organic phosphorus: a review of world literature. CAB International, WallingfordGoogle Scholar
  25. Hayes JE, Richardson AE, Simpson RJ (2000) Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase. Biol Fertil Soils 32:279–286. CrossRefGoogle Scholar
  26. Haygarth PM, Harrison AF, Turner BL (2018) On the history and future of soil organic phosphorus research: a critique across three generations. Eur J Soil Sci 69:86–94. CrossRefGoogle Scholar
  27. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195. CrossRefGoogle Scholar
  28. Irving GCJ, Cosgrove DJ (1981) The use of hypobromite oxidation to evaluate two current methods for the estimation of inositol polyphosphates in alkaline extracts of soils. Commun Soil Sci Plant Anal 12:495–509. CrossRefGoogle Scholar
  29. Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44. CrossRefGoogle Scholar
  30. Karathanasis AD, Shumaker PD (2009) Organic and inorganic phosphate interactions with soil hydroxy-interlayered minerals. J Soils Sediments 9:501–510. CrossRefGoogle Scholar
  31. Lagos LM, Acuña JJ, Maruyama F, Ogram A, de la Luz Mora M, Jorquera MA (2016) Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fertil Soils 52:1007–1019. CrossRefGoogle Scholar
  32. Li M, Osaki M, Madhusudana Rao I, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195:161–169. CrossRefGoogle Scholar
  33. Lienhard P, Tivet F, Chabanne A, Dequiedt S, Lelièvre M, Sayphoummie S, Leudphanane B, Prévost-Bouré NC, Séguy L, Maron P-A, Ranjard L (2012) No-till and cover crops shift soil microbial abundance and diversity in Laos tropical grasslands. Agron Sustain Dev 33:375–384. CrossRefGoogle Scholar
  34. Louw-Gaume AE, Rao IM, Gaume AJ, Frossard E (2010) A comparative study on plant growth and root plasticity responses of two Brachiaria forage grasses grown in nutrient solution at low and high phosphorus supply. Plant Soil 328:155–164. CrossRefGoogle Scholar
  35. Louw-Gaume AE, Schweizer N, Rao IM, Gaume AJ, Frossard E (2017) Temporal differences in plant growth and root exudation of two Brachiaria grasses in response to low phosphorus supply. Trop Grasslands 5:103–116. CrossRefGoogle Scholar
  36. Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388. CrossRefGoogle Scholar
  37. MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world’s croplands. P Natl Acad Sci U S A 108:3086–3091. CrossRefGoogle Scholar
  38. Margenot AJ, Sommer R, Mukalama J, Parikh SJ (2017) Biological P cycling is influenced by the form of P fertilizer in an Oxisol. Biol Fertil Soils 53:899–909. CrossRefGoogle Scholar
  39. Martin M, Celi L, Barberis E (2004) Desorption and plant availability of myo-inositol hexaphosphate adsorbed on goethite. Soil Sci 169:115–124CrossRefGoogle Scholar
  40. Menezes-Blackburn D, Jorquera MA, Greiner R, Gianfreda L, de la Luz Mora M (2013) Phytases and phytase–labile organic phosphorus in manures and soils. Crit Rev Environ Sci Technol 43:916–954. CrossRefGoogle Scholar
  41. Menezes-Blackburn D, Paredes C, Zhang H, Giles CD, Darch T, Stutter M, George TS, Shand C, Lumsdon D, Cooper P, Wendler R, Brown L, Blackwell M, Wearing C, Haygarth PM (2016) Organic acids regulation of chemical–microbial phosphorus transformations in soils. Environ Sci Technol 50:11521–11531. CrossRefPubMedGoogle Scholar
  42. Menezes-Blackburn D, Giles C, Darch T, George TS, Blackwell M, Stutter M, Shand C, Lumsdon D, Cooper P, Wendler R, Brown L, Almeida DS, Wearing C, Zhang H, Haygarth PM (2017) Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review. Plant Soil 427:1–18. CrossRefGoogle Scholar
  43. Merlin A, He ZL, Rosolem CA (2014) Congo grass grown in rotation with soybean affects phosphorus bound to soil carbon. Rev Bras Cienc Solo 38:888–895. CrossRefGoogle Scholar
  44. Merlin A, Rosolem CA, He ZL (2015) Non-labile phosphorus acquisition by Brachiaria. J Plant Nutr 39:1319–1327. CrossRefGoogle Scholar
  45. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, pp 215–243. CrossRefGoogle Scholar
  46. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191. CrossRefGoogle Scholar
  47. Olibone D, Rosolem CA (2010) Phosphate fertilization and phosphorus forms in an Oxisol under no-till. Sci Agric 67:465–471. CrossRefGoogle Scholar
  48. Onthong J, Osaki M (2006) Adaptations of tropical plants to acid soils. Tropics 15:337–347. CrossRefGoogle Scholar
  49. Raij B, Quaggio JA, Da Silva NM (1986) Extraction of phosphorus, potassium, calcium, and magnesium from soils by an ion-exchange resin procedure. Commun Soil Sci Plant Anal 17:547–566. CrossRefGoogle Scholar
  50. Rao IM, Kerridge PC, Macedo MCM (1996) Nutritional requirements of Brachiaria and adaptation to acid soils. In: Miles JW, Maass BL, do Valle CB (eds) Brachiaria: biology, agronomy and improvement. CIAT/EMBRAPA, Cali, pp 53–71Google Scholar
  51. Redel YD, Rubio R, Rouanet JL, Borie F (2007) Phosphorus bioavailability affected by tillage and crop rotation on a Chilean volcanic derived Ultisol. Geoderma 139:388–396. CrossRefGoogle Scholar
  52. Richardson AE, Hadobas PA, Hayes JE, O’Hara CP, Simpson RJ (2001) Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil micro-organisms. Plant Soil 229:47–56. CrossRefGoogle Scholar
  53. Rodrigues M, Pavinato PS, Withers PJA, Teles APB, Herrera WFB (2016) Legacy phosphorus and no tillage agriculture in tropical Oxisols of the Brazilian savanna. Sci Total Environ 542:1050–1061. CrossRefPubMedGoogle Scholar
  54. Rosolem CA, Merlin A, Bull JCL (2014) Soil phosphorus dynamics as affected by congo grass and P fertilizer. Sci Agric 71:309–315. CrossRefGoogle Scholar
  55. Shang C, Caldwell DE, Stewart JWB, Tiessen H, Huang PM (1996) Bioavailability of organic and inorganic phosphates adsorbed on short-range ordered aluminum precipitate. Microb Ecol 31:29–39. CrossRefPubMedGoogle Scholar
  56. Shears SB, Turner BL (2007) Nomenclature and terminology of inositol phosphates: clarification and a glossary of terms. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, pp 1–6Google Scholar
  57. Shoemaker HE, McLean EO, Pratt PF (1961) Buffer methods for determining lime requirement of soils with appreciable amounts of extractable aluminum. Soil Sci Soc Am J 25:274–277. CrossRefGoogle Scholar
  58. Simon CA, Cordeiro MS, SFd L, Brasil MS, David CHD, Secco VA (2017) Microbial activity in a soil with cover crops in succession with maize in a no-tillage system. Braz J Agric 92:198–207Google Scholar
  59. Soil Survey Staff (2014) Keys to soil taxonomy, 12th edn. USDA-Natural Resources Conservation Service, Washington, DCGoogle Scholar
  60. Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochemistry 4:41–60. CrossRefGoogle Scholar
  61. Turner BL, Richardson AE (2004) Identification of scyllo-inositol phosphates in soil by solution phosphorus-31 nuclear magnetic resonance spectroscopy. Soil Sci Soc Am J 68:802–808. CrossRefGoogle Scholar
  62. Turner BL, Papházy MJ, Haygarth PM, Mckelvie ID (2002) Inositol phosphates in the environment. Philos Trans R Soc B 357:449–469. CrossRefGoogle Scholar
  63. Turner BL, Cheesman AW, Godage HY, Riley AM, Potter BVL (2012) Determination of neo- and D-chiro-inositol hexakisphosphate in soils by solution (31)P NMR spectroscopy. Environ Sci Technol 46:4994–5002. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Van Veldhoven PP, Mannaerts GP (1987) Inorganic and organic phosphate measurements in the nanomolar range. Anal Biochem 161:45–48. CrossRefPubMedGoogle Scholar
  65. Walkley A, Black IA (1934) An examination of the degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38. CrossRefGoogle Scholar
  66. Wenzl P, Patino GM, Chaves AL, Mayer JE, Rao IM (2001) The high level of aluminum resistance in signalgrass is not associated with known mechanisms of external aluminum detoxification in root apices. Plant Physiol 125:1473–1484. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wyss M, Brugger R, Kronenberger A, Rémy R, Fimbel R, Oesterhelt G, Lehmann M, van Loon APGM (1999) Biochemical characterization of fungal phytases (myo-inositol hexakisphosphate phosphohydrolases): catalytic properties. Appl Environ Microbiol 65:367–373PubMedPubMedCentralGoogle Scholar
  68. Yadav BK, Tarafdar JC (2004) Phytase activity in the rhizosphere of crops, trees and grasses under arid environment. J Arid Environ 58:285–293. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Danilo S. Almeida
    • 1
    Email author
  • Daniel Menezes-Blackburn
    • 2
    • 3
  • Benjamin L. Turner
    • 4
  • Catherine Wearing
    • 2
  • Philip M. Haygarth
    • 2
  • Ciro A. Rosolem
    • 1
  1. 1.College of Agricultural Sciences, Department of Crop ScienceSão Paulo State UniversityBotucatuBrazil
  2. 2.Lancaster Environment CentreLancaster UniversityLancasterUK
  3. 3.Department of Soils, College of Agricultural and Marine Sciences, Water and Agricultural EngineeringSultan Qaboos UniversityAl-khodSultanate of Oman
  4. 4.Smithsonian Tropical Research InstituteAnconRepublic of Panama

Personalised recommendations