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Plant and Soil

, Volume 412, Issue 1–2, pp 43–59 | Cite as

Does the combination of citrate and phytase exudation in Nicotiana tabacum promote the acquisition of endogenous soil organic phosphorus?

  • Courtney D. Giles
  • Timothy S. George
  • Lawrie K. Brown
  • Malika M. Mezeli
  • Alan E. Richardson
  • Charles A. Shand
  • Renate Wendler
  • Tegan Darch
  • Daniel Menezes-Blackburn
  • Patricia Cooper
  • Marc I. Stutter
  • David G. Lumsdon
  • Martin S. A. Blackwell
  • Catherine Wearing
  • Hao Zhang
  • Philip M. Haygarth
Regular Article

Abstract

Background and Aims

Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants.

Methods

N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter (A. thaliana frd3) or fungal phytases (phyA: A. niger, P. lycii) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linear-regression was used to predict shoot P accumulation based on plant exudation and soil P depletion.

Results

Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P < .0001). Positive complementarity occurred between intercropped citrate- and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression.

Conclusions

We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.

Keywords

Complementarity Root exudation Rhizosphere Citrate Phytase Soil organic phosphorus 

Notes

Acknowledgments

We would like to acknowledge David Lewis (CSIRO Agriculture, Canberra Australia) for developing the crossed lines of tobacco, Susan McIntyre and Fiona Sturgeon (James Hutton Institute, Aberdeen, UK) for their contribution to the analysis of soils, and Katharine Preedy (BioSS, James Hutton Institute, Dundee, UK) for statistical consultation. Funding for this research was provided through a BBSRC responsive mode grant (BBK0170471).

Supplementary material

11104_2016_2884_MOESM1_ESM.pdf (599 kb)
Online Resource 1 (PDF 624 kb)
11104_2016_2884_MOESM2_ESM.pdf (374 kb)
Online Resource 2 (PDF 385 kb)
11104_2016_2884_MOESM3_ESM.pdf (374 kb)
Online Resource 3 (PDF 385 kb)

References

  1. Bolan NS, Naidu R, Mahimairaja S, Baskaran S (1994) Influence of low-molecular-weight organic acids on the solubilization of phosphate. Biology and Fertility of Soils 18:311–319CrossRefGoogle Scholar
  2. Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CAB International Inc., Wallingford, pp. 113–132Google Scholar
  3. Chen R, Xue G, Chen P, Yao B, Yang W, Ma Q, Fan Y, Zhao Z, Tarczynski MC, Shi J (2008) Transgenic maize plants expressing a fungal phytase gene. Transgenic research 17:633–643. doi: 10.1007/s11248-007-9138-3 CrossRefPubMedGoogle Scholar
  4. Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal-stabilized soil organic matter – The unbutton model. Soil Biol Biochem 84:168–176. doi: 10.1016/j.soilbio.2015.02.019 CrossRefGoogle Scholar
  5. Condron LM, Spears BM, Haygarth PM, Turner BL, Richardson AE (2013) Role of legacy phosphorus in improving global phosphorus-use efficiency. Environ Dev 8:147–148. doi: 10.1016/j.envdev.2013.09.003 CrossRefGoogle Scholar
  6. Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. The Plant cell 14:1347–1357CrossRefPubMedPubMedCentralGoogle Scholar
  7. Dagley S (1974) Citrate: UV spectrophotometric determination. In: H Bergmeyer (ed) Methods of Enzymatic Analysis. Academic Press, New YorkGoogle Scholar
  8. Dissanayaka D, Maruyama H, Masuda G, Wasaki J (2015) Interspecific facilitation of P acquisition in intercropping of maize with white lupin in two contrasting soils as influenced by different rates and forms of P supply. Plant and Soil 390:223–236. doi: 10.1007/s11104-015-2392-x
  9. FAO (2014) World reference base for soil resources 2014: International soil reference system for naming soils and creating legends for soil maps. World Soil Resources Reports: 106. Food and Agriculture Organization of the United Nations, Global Soil Partnership, International Union of Soil Sciences, Rome, p 203Google Scholar
  10. George TS, Gregory PJ, Robinson JS, Buresh RJ (2002) Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant and Soil 246:65–73. doi: 10.1023/a:1021523515707 CrossRefGoogle Scholar
  11. George TS, Richardson AE, Hadobas PA, Simpson RJ (2004) Characterization of transgenic Trifolium subterraneum L. wwhich expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil. Plant, Cell & Environment 27:1351–1361. doi: 10.1111/j.1365-3040.2004.01225.x CrossRefGoogle Scholar
  12. George TS, Simpson RJ, Hadobas PA, Richardson AE (2005) Expression of a fungal phytase gene in Nicotiana tabacum improves phosphorus nutrition of plants grown in amended soils. Plant Biotechnol J 3:129–140. doi: 10.1111/j.1467-7652.2004.00116.x CrossRefPubMedGoogle Scholar
  13. George TS, Turner BL, Gregory PJ, Cade-Menun BJ, Richardson AE (2006) Depletion of organic phosphorus from Oxisols in relation to phosphatase activities in the rhizosphere. Eur J Soil Sci 57:47–57. doi: 10.1111/j.1365-2389.2005.00767.x CrossRefGoogle Scholar
  14. George T, Quiquampoix H, Simpson R, Richardson A (2007a) Interactions Between Phytases and Soil Constituents: Implicatins for the Hydrolysis of Inositol Phosphates. In: Turner B, Richardson A, Mullaney E (eds) Inositol Phosphates: Linking Agriculture and the Environment. CABI, Oxfordshire, UKGoogle Scholar
  15. George TS, Simpson RJ, Gregory PJ, Richardson AE (2007b) Differential interaction of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates. Soil Biology & Biochemistry 39:793–803. doi: 10.1016/j.soilbio.2006.09.029
  16. George TS, Richardson, AE, Sumei L, Gregory PJ, Daniell TD (2009) Extracellular release of a heterologous phytase from roots of transgenic plants: does manipulation of rhizosphere biochemistry impact microbial community structure? FEMS Microbiology Ecology 70:433–445Google Scholar
  17. 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. doi: 10.1016/j.soilbio.2009.12.002 CrossRefGoogle Scholar
  18. Giles CD, Cade-Menun B (2014) Phytate in animal manure and soils: abundance, cycling and bioavailability. In: He Z, Zhang H (eds) Applied manure and nutrient chemistry for sustainable agriculture and environment. Springer, New YorkGoogle Scholar
  19. Giles CD, Richardson AE, Druschel GK, Hill JE (2012) Organic anion-driven solubilization of precipitated and sorbed phytate improves hydrolysis by phytases and bioavailability to Nicotiana tabacum. Soil Sci 177:591–598CrossRefGoogle Scholar
  20. Greiner R (2007) Phytate-degrading enzymes: regulation of synthesis in microorganisms and plants. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Oxfordshire, UKGoogle Scholar
  21. Hauggaard-Nielsen H, Jensen ES (2005) Facilitative root interactions in intercrops. In: Lambers H, Colmer T (eds) Root physiology: from Gene to function Springer NetherlandsGoogle Scholar
  22. 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 32:279–286CrossRefGoogle Scholar
  23. Heffernan B (1985) A handbook of methods of inorganic chemical analysis for forest soils, foliage and water. CSIRO Division of Forest Research, Canberra ACTGoogle Scholar
  24. Irving GCJ, McLaughlin MJ (1990) A rapid and simple field test for phosphorus in Olsen and Bray no. 1 extracts of soil. Commun Soil Sci Plant Anal 21:2245–2255. doi: 10.1080/00103629009368377 CrossRefGoogle Scholar
  25. Lassen SF, Breinholt J, Østergaard PR, Brugger R, Bischoff A, Wyss M, Fuglsang CC (2001) Expression, Gene cloning, and characterization of five novel Phytases from four basidiomycete fungi: Peniophora lycii, Agrocybe pediades, a Ceriporia sp., and Trametes pubescens. Appl Environ Microbiol 67:4701–4707. doi: 10.1128/aem.67.10.4701-4707.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Li L, Yang S, Li X, Zhang F, Christie P (1999) Interspecific complementary and competitive interactions between intercropped maize and faba bean. Plant Soil 212:105–114. doi: 10.1023/A:1004656205144 CrossRefGoogle Scholar
  27. Li L, Tang C, Rengel Z, Zhang F (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248:297–303. doi: 10.1023/A:1022389707051 CrossRefGoogle Scholar
  28. Li L, Tang C, Rengel Z, Zhang FS (2004) Calcium, magnesium and microelement uptake as affected by phosphorus sources and interspecific root interactions between wheat and chickpea. Plant Soil 261:29–37. doi: 10.1023/B:PLSO.0000035579.39823.16 CrossRefGoogle Scholar
  29. Lung S-C, Chan W-L, Yip W, Wang L, Yeung EC, Lim BL (2005) Secretion of beta-propeller phytase from tobacco and Arabidopsis roots enhances phosphorus utilization. Plant Sci 169:341–349. doi: 10.1016/j.plantsci.2005.03.006 CrossRefGoogle Scholar
  30. Lynch JP (2007) Rhizoeconomics: the roots of shoot growth limitations. Hortscience 42:1107–1109Google Scholar
  31. Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. doi: 10.1104/pp.111.175414 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56. doi: 10.1007/s11104-004-1096-4 CrossRefGoogle Scholar
  33. Ma X-F, Tudor S, Butler T, Ge Y, Xi Y, Bouton J, Harrison M, Wang Z-Y (2012) Transgenic expression of phytase and acid phosphatase genes in alfalfa (Medicagosativa) leads to improved phosphate uptake in natural soils. Mol Breed 30:377–391. doi: 10.1007/s11032-011-9628-0 CrossRefPubMedGoogle Scholar
  34. Menezes-Blackburn D, Jorquera MA, Greiner R, Gianfreda L, Mora MD (2013) Phytases and Phytase-labile organic phosphorus in manures and soils. Crit Rev Environ Sci Technol 43:916–954. doi: 10.1080/10643389.2011.627019 CrossRefGoogle Scholar
  35. Menezes-Blackburn D, Gabler S, Greiner R (2015) Performance of seven commercial Phytases in an in vitro simulation of poultry digestive tract. J Agric Food Chem 63:6142–6149. doi: 10.1021/acs.jafc.5b01996 CrossRefPubMedGoogle Scholar
  36. Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between root hair length and basal root growth Angle for phosphorus acquisition. Plant Physiol 167:1430–1439. doi: 10.1104/pp.15.00145 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mudge SR, Smith FW, Richardson AE (2003) Root-specific and phosphate-regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole P source. Plant Sci 165:871–878. doi: 10.1016/S0168-9452(03)00286-3 CrossRefGoogle Scholar
  38. Reuter D, Robinson J (eds) (1997) Plant analysis: an interpretation manual. CSIRO Publishing, Collingwood, p 450Google Scholar
  39. 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 23:397–405. doi: 10.1046/j.1365-3040.2000.00557.x CrossRefGoogle Scholar
  40. Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J CellMol Biol 25:641–649Google Scholar
  41. 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 349:121–156. doi: 10.1007/s11104-011-0950-4 CrossRefGoogle Scholar
  42. Ryan MH, Tibbett M, Edmonds-Tibbett T, Suriyagoda LD, Lambers H, Cawthray GR, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180. doi: 10.1111/j.1365-3040.2012.02547.x CrossRefPubMedGoogle Scholar
  43. Ryan PR, James RA, Weligama C, Delhaize E, Rattey A, Lewis DC, Bovill WD, McDonald G, Rathjen TM, Wang E, Fettell NA, Richardson AE (2014) Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat. Physiol Plant 151:230–242. doi: 10.1111/ppl.12150 CrossRefPubMedGoogle Scholar
  44. Schunmann PHD, Surin B, Waterhouse PM (2003) A suite of novel promoters and terminators for plant biotechnology. II. The pPLEX series for use in monocots. Funct Plant Biol 30:453–460. doi: 10.1071/FP02167 CrossRefGoogle Scholar
  45. Shen J, Li C, Mi G, Li L, Yuan L, Jiang R, Zhang F (2013) Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J Exp Bot 64:1181–1192CrossRefPubMedGoogle Scholar
  46. Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R, MacKay RL, Richardson AE, Condron LM, Turner BL, Haygarth PM (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978. doi: 10.1021/es2044745 CrossRefPubMedGoogle Scholar
  47. Stutter MI, Shand CA, George TS, Blackwell MSA, Dixon L, Bol R, MacKay RL, Richardson AE, Condron LM, Haygarth PM (2015) Land use and soil factors affecting accumulation of phosphorus species in temperate soils. Geoderma 257–258:29–39. doi: 10.1016/j.geoderma.2015.03.020 CrossRefGoogle Scholar
  48. Tang J, Leung A, Leung C, Lim BL (2006) Hydrolysis of precipitated phytate by three distinct families of phytases. Soil Biol Biochem 38:1316–1324. doi: 10.1016/j.soilbio.2005.08.021 CrossRefGoogle Scholar
  49. Ullah AHJ, Sethumadhavan K (2003) PhyA gene product of Aspergillus ficuum and Peniophora lycii produces dissimilar phytases. Biochem Biophys Res Commun 303:463–468. doi: 10.1016/S0006-291X(03)00374-7 CrossRefPubMedGoogle Scholar
  50. Vats P, Banerjee UC (2004) Production studies and catalytic properties of phytases (myo-inositolhexakisphosphate phosphohydrolases): an overview. Enzym Micro Technol 35:3–14. doi: 10.1016/j.enzmictec.2004.03.010 CrossRefGoogle Scholar
  51. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51. doi: 10.1104/pp.102.019661 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wang Y, Ye X, Ding G, Xu F (2013) Overexpression of phyA and appA genes improves soil organic phosphorus utilisation and seed Phytase activity in Brassica napus. PLoS One 8:e60801–e60801. doi: 10.1371/journal.pone.0060801 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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
  54. Yan YP, Liu F, Li W, Liu F, Feng XH, Sparks DL (2014) Sorption and desorption characteristics of organic phosphates of different structures on aluminium (oxyhydr)oxides. Eur J Soil Sci 65:308–317. doi: 10.1111/ejss.12119 CrossRefGoogle Scholar
  55. Zhang F, Li L (2003) Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248:305–312. doi: 10.1023/A:1022352229863 CrossRefGoogle Scholar
  56. Zhang C, Postma JA, York LM, Lynch JP (2014) Root foraging elicits niche complementarity-dependent yield advantage in the ancient ‘three sisters’ (maize/bean/squash) polyculture. Ann Bot 114:1719–1733. doi: 10.1093/aob/mcu191 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zimmermann P, Zardi G, Lehmann M, Zeder C, Amrhein N, Frossard E, Bucher M (2003) Engineering the root–soil interface via targeted expression of a synthetic phytase gene in trichoblasts. Plant Biotechnol J 1:353–360. doi: 10.1046/j.1467-7652.2003.00033.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Courtney D. Giles
    • 1
  • Timothy S. George
    • 1
  • Lawrie K. Brown
    • 1
  • Malika M. Mezeli
    • 1
  • Alan E. Richardson
    • 3
  • Charles A. Shand
    • 2
  • Renate Wendler
    • 2
  • Tegan Darch
    • 4
  • Daniel Menezes-Blackburn
    • 5
  • Patricia Cooper
    • 2
  • Marc I. Stutter
    • 2
  • David G. Lumsdon
    • 2
  • Martin S. A. Blackwell
    • 4
  • Catherine Wearing
    • 5
  • Hao Zhang
    • 5
  • Philip M. Haygarth
    • 5
  1. 1.James Hutton Institute:Dundee DD2 5DAUK
  2. 2.James Hutton Institute:Aberdeen AB15 8QHUK
  3. 3.CSIRO AgricultureCanberra ACTAustralia
  4. 4.Rothamsted ResearchOkehamptonUK
  5. 5.Lancaster Environment CentreLancaster UniversityLancasterUK

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