Plant and Soil

, Volume 354, Issue 1–2, pp 283–298 | Cite as

Phosphorus pools and other soil properties in the rhizosphere of wheat and legumes growing in three soils in monoculture or as a mixture of wheat and legume

Regular Article

Abstract

Background and aims

Phosphorus and nitrogen availability and forms are affected by soil properties as well as by plant species and further modulated by soil microbes. Additionally, close contact of the roots of two plant species may affect concentrations and forms of N and P. The aim of this study was to assess properties related to N and P cycling in the rhizosphere of wheat and legumes grown in monoculture or in wheat/legume mixtures in three soils differing in pH.

Methods

Faba bean, white lupin and wheat were grown in three soils differing in pH (4.8, 7.5 and 8.8) in monoculture or in mixed culture of wheat and legumes. Rhizosphere soil was collected at flowering and analyzed for P pools by sequential fractionation, available N as well as community structure of bacteria, fungi, ammonia oxidizers, N2-fixers and P mobilizers by polymerase chain reaction (PCR)—denaturing gradient gel electrophoresis (DGGE).

Results

Soil type was the major factor determining plant growth, rhizosphere nutrient dynamics and microbial community structure. Among the crop species, only faba bean had a significant effect on nitrification potential activity (PNA) in all three soils with lower activity compared to the unplanted soil. Soil type and plant spieces affected the community composition of ammonia-oxidizing archaea (AOB), ammonia-oxidizing archaea (AOA), N2-fixers (nifH), P mobilizers (ALP gene) and fungi, but not that of bacteria. Among the microbial groups, the AOA and nifH community composition were most strongly affected by crop species, cropping system and soil type, suggesting that these groups are quite sensitive to environmental conditions. All plants depleted some labile as well as non-labile P pools whereas the less labile organic P pools (NaOH extractable P pools, acid extractable P pools) accumulated in the rhizosphere of legumes. The pattern of depletion and accumulation of some P pools differed between monoculture and mixed culture as well as among soils.

Conclusions

Plant growth and rhizosphere properties were mainly affected by soil type, but also by crop species whereas cropping system had the least effect. Wheat and the legumes depleted less labile inorganic P pools in some soils whereas less labile organic P pools (NaOH extractable P, acid extractable P) accumulated in the rhizosphere of legumes.

Keywords

Legumes Microbial community Mixed culture Nitrogen Phosphorus pools pH Rhizosphere Wheat 

Notes

Acknowledgement

We thank Collin Rivers for his help of collecting the soils from Monarto and Mt. Bold and Sean Mason for collecting the Langhorne Creek soil. We are grateful to the financial support from the Australian Research Council, and the China Scholarship Council.

References

  1. Ae N, Arihara J, Okada K (1990) Phosphorus uptake by piegeon pea and its role in cropping systems of the Indian subcontinent. Science 248:477–480PubMedCrossRefGoogle Scholar
  2. Anderson IC, Campbell CD, Prosser JI (2003) Diversity of fungi in organic soils under a moorland—Scots pine (Pinus sylvestris L.) gradient. Environ Microbiol 5:1121–1132PubMedCrossRefGoogle Scholar
  3. Bagayoko M, Alvey S, Neumann G, Buerkert A (2000) Root-induced increases in soil pH and nutrient availability to field-grown cereals and legumes on acid sandy soils of Sudano-Sahelian West Africa. Plant Soil 225:117–127CrossRefGoogle Scholar
  4. Bhat KKS, Nye PH (1973) Diffusion of phosphate to plant roots in soil. I. Quantitative autoradiography of the depletion zone. Plant Soil 38:161–175CrossRefGoogle Scholar
  5. Bissett A, Burke C, Cook PLM, Bowman JP (2007) Bacterial community shifts in organically perturbed sediments. Environ Microbiol 9:46–60PubMedCrossRefGoogle Scholar
  6. Bowman GM, Hutka J (2002) Particle size analysis. In: McKenzie N, Coughlan K, Cresswell H (eds) Soil physical measurement and interpretation for land evaluation. CSIRO, Collingwood, pp 224–239Google Scholar
  7. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research, CanberraGoogle Scholar
  8. Chen X, Zhang L-M, Shen J-P, Xu Z, He J-Z (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516CrossRefGoogle Scholar
  9. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, PlymouthUKGoogle Scholar
  10. Coelho MRR, de Vos M, Carneiro NP, Marriel IE, Paiva E, Seldin L (2008) Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum (Sorghum bicolor) treated with contrasting levels of nitrogen fertilizer. FEMS Microbiol Lett 279:15–22PubMedCrossRefGoogle Scholar
  11. Condron LM, Goh KM (1989) Effects of long-term phosphatic fertilizer applications on amounts and forms of phosphorus in soils under irrigated pasture in New Zealand. J Soil Sci 40:383–395CrossRefGoogle Scholar
  12. Cu STT, Hutson J, Schuller KA (2005) Mixed culture of wheat (Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant Soil 272:143–151CrossRefGoogle Scholar
  13. Diallo MD, Willems A, Vloemans N, Cousin S, Vandekerckhove TT, de Lajudie P, Neyra M, Vyverman W, Gillis M, Van der Gucht K (2004) Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N-2-fixing bacterial diversity in soil under Acacia tortilis ssp raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ Microbiol 6:400–415CrossRefGoogle Scholar
  14. Fan FL, Zhang FS, Lu YH (2010) Linking plant identity and interspecific competition to soil nitrogen cycling through ammonia oxidizer communities. Soil Biol Biochem 43:46–54CrossRefGoogle Scholar
  15. Feng X, Nielsen LL, Simpson MJ (2007) Responses of soil organic matter and microorganisms to freeze-thaw cycles. Soil Biology and Biochemistry 39:2027–2037CrossRefGoogle Scholar
  16. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631PubMedCrossRefGoogle Scholar
  17. Fierer N, Carney KM, Horner-Devine MC, Megonigal JP (2009) The biogeography of ammonia-oxidizing bacterial communities in soil. Microb Ecol 58:435–445PubMedCrossRefGoogle Scholar
  18. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688PubMedCrossRefGoogle Scholar
  19. George TS, Gregory PJ, Hocking P, Richardson AE (2008) Variation in root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the P-nutrition of plants when grown in soils. Environ Exp Bot 64:239–249CrossRefGoogle Scholar
  20. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  21. Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976CrossRefGoogle Scholar
  22. Henrikson A, Selmer-Olsen AR (1970) Automatic methods for determining nitrate and nitrite in water and soil extracts. Analyst 95(514)Google Scholar
  23. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  24. Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239CrossRefGoogle Scholar
  25. Hu J, Lin X, Wang J, Cui X, Dai J, Chu H, Zhang J (2010) Arbuscular mycorrhizal fungus enhances P acquisition of wheat (Triticum aestivum L.) in a sandy loam soil with long-term inorganic fertilization regime. Appl Microbiol Biotechnol 88:781–787PubMedCrossRefGoogle Scholar
  26. Joergensen RG, Brookes PC (1990) Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts. Soil Biol Biochem 22:1023–1027CrossRefGoogle Scholar
  27. Klotz MG, Stein LY (2008) Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol Lett 278:146–156PubMedCrossRefGoogle Scholar
  28. Kouno K, Information C, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method Soil Biol Biochem 27:1353–1357Google Scholar
  29. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529PubMedCrossRefGoogle Scholar
  30. Kuo S (1996) Phosphorus. In: Spark DL (ed) Methods of soil analysis, 3rd edn. Soil Science Society of America, Madison, pp 869–919Google Scholar
  31. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103PubMedCrossRefGoogle Scholar
  32. Li L, Tang CX, Rengel Z, Zhang FS (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant and Soil 248:297–303CrossRefGoogle Scholar
  33. Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot 94:297–303PubMedCrossRefGoogle Scholar
  34. Li L, Li S-M, Sun J-H, Zhou L-L, Bao X-G, Zhang H-G, Zhang F-S (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci USA 104:11192–11196PubMedCrossRefGoogle Scholar
  35. Li J, Xie Y, Dai A, Liu L, Li Z (2009) Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice. J Genet Genomics 36:173–183PubMedCrossRefGoogle Scholar
  36. Li HG, Shen JB, Zhang FS, Marschner P, Cawthray G, Rengel Z (2011) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biol Fertil Soils 46:79–91CrossRefGoogle Scholar
  37. Lindsay WL (1979) Chemical equilibria in soils. Wiley, New York, 449pGoogle Scholar
  38. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13PubMedGoogle Scholar
  39. Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237CrossRefGoogle Scholar
  40. Mahmood S, Prosser JI (2006) The influence of synthetic sheep urine on ammonia oxidizing bacterial communities in grassland soil. FEMS Microbiol Ecol 56:444–454PubMedCrossRefGoogle Scholar
  41. Marschner P, Solaiman Z, Rengel Z (2005) Growth, phosphorus uptake and rhizosphere microbial community composition of a phosphorus-efficient wheat cultivar in soils differing in pH. J Plant Nutrit Soil Sci 168:343–351Google Scholar
  42. Mohammad MJ, Pan WL, Kennedy AC (2005) Chemical alteration of the rhizosphere of the mycorrhizal-colonized wheat root. Mycorrhiza 15:259–266PubMedCrossRefGoogle Scholar
  43. Moisander PH, Morrison AE, Ward BB, Jenkins BD, Zehr JP (2007) Spatial-temporal variability in diazotroph assemblages in Chesapeake Bay using an oligonucleotide nifH microarray. Environ Microbiol 9:1823–1835PubMedCrossRefGoogle Scholar
  44. Murphy J, Riley J (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27:31–36CrossRefGoogle Scholar
  45. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedGoogle Scholar
  46. Nicolaisen MH, Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Meth 50:189–203CrossRefGoogle Scholar
  47. Nugroho RA, Roling WF, Laverman AM, Verhoef HA (2007) Low nitrification rates in acid Scots pine forest soils are due to pH-related factors. Microb Ecol 53:89–97PubMedCrossRefGoogle Scholar
  48. Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120CrossRefGoogle Scholar
  49. Ortas I, Rowell DL (2004) Effect of ammonium and nitrate on indigenous mycorrhizal infection, rhizosphere pH change, and phosphorus uptake by sorghum. Commun Soil Sci Plant Anal 35:1923–1944CrossRefGoogle Scholar
  50. Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103PubMedCrossRefGoogle Scholar
  51. Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods. Inkata, Melbourne, pp 1–23Google Scholar
  52. Reuter DJ, Robinson JB (1997) Plant analysis: an interpretation manual. CSIRO, CollingwoodGoogle Scholar
  53. Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant Cell Environ 23:397–405CrossRefGoogle Scholar
  54. Rose TJ, Hardiputra B, Rengel Z (2010) Wheat, canola and grain legume access to soil phosphorus fractions differs in soils with contrasting phosphorus dynamics. Plant Soil 326:159–170CrossRefGoogle Scholar
  55. Rousk J, Brookes PC, Baath E (2009) Contrasting soil pH efects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596PubMedCrossRefGoogle Scholar
  56. Rousk J, Baath E, Brookes PC, Lauber CL, Laozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351PubMedCrossRefGoogle Scholar
  57. Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71CrossRefGoogle Scholar
  58. Searle PL (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. Analyst A Rev 109:549–568Google Scholar
  59. Sen S, Mukherji S (2004) Alterations in activities of acid phosphatase, alkaline phosphatase, ATPase and ATP content in response to seasonally varying Pi status in okra (Abelmoschus esculentus). J Environ Biol 25:181–185PubMedGoogle Scholar
  60. Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611PubMedCrossRefGoogle Scholar
  61. Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet 109:1361–1368PubMedCrossRefGoogle Scholar
  62. Starnes DL, Padmanabhan P, Sahi SV (2008) Effect of P sources on growth, P accumulation and activities of phytase and acid phosphatases in two cultivars of annual ryegrass (Lolium multiflorum L.). Plant Physiol Biochem 46:580–589CrossRefGoogle Scholar
  63. Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochemistry 4:41–60CrossRefGoogle Scholar
  64. Tang C, Mclay CDA, Barton L (1997) A comparison of proton excretion of twelve pasture legumes grown in nutrient solution. Aust J Exp Agric 37:563–570CrossRefGoogle Scholar
  65. Tiessen H, Moir JO (1993) Charaterisation of available P by sequential extration. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, Boca Raton, pp 104–107Google Scholar
  66. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedGoogle Scholar
  67. Vu DT, Tang C, Armstrong RD (2008) Changes and availability of P fractions following 65 years of P application to a calcareous soil in a Mediterranean climate. Plant Soil 304:21–33CrossRefGoogle Scholar
  68. 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 Science 37:29–38CrossRefGoogle Scholar
  69. Wang BL, Shen JB, Zhang WH, Zhang FS, Neumann G (2007) Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytol 176:581–589PubMedCrossRefGoogle Scholar
  70. Wang Y, Hasbullah, Setia R, Marschner P, Zhang F (2011) Potential soil P mobilisation capacity—method development and comparison of rhizosphere soil from different crops. Plant Soil (in press).Google Scholar
  71. Wilke BM (2005) Determination of chemical and physical soil properties. In: Margesin R, Schinner F (eds) Manual for soil analysis—monitoring and assessing soil bioremediation. Springer, Berlin, pp 47–93CrossRefGoogle Scholar
  72. Wu YC, Lu L, Wang BZ, Lin XG, Zhu JG, Cai ZC, Yan XY, Jia ZJ (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75:1431–1439CrossRefGoogle Scholar
  73. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132PubMedCrossRefGoogle Scholar
  74. Zhang YG, Li DQ, Wang HM, Xiao QM, Liu XD (2006) Molecular diversity of nitrogen-fixing bacteria from the Tibetan Plateau, China. FEMS Microbiol Lett 260:134–142PubMedCrossRefGoogle Scholar
  75. Zhang YY, Dong JD, Yang ZH, Zhang S, Wang YS (2008) Phylogenetic diversity of nitrogen-fixing bacteria in mangrove sediments assessed by PCR-denaturing gradient gel electrophoresis. Arch Microbiol 190:19–28PubMedCrossRefGoogle Scholar
  76. Zhu Y, Yan F, Zorb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46:892–901PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.College of Resources and Environmental SciencesChina Agricultural UniversityBeijingChina
  2. 2.School of Agriculture, Food and Wine, The Waite Research InstituteThe University of AdelaideAdelaideAustralia

Personalised recommendations