Advertisement

Plant and Soil

, Volume 358, Issue 1–2, pp 91–104 | Cite as

Phosphorus supply enhances the response of legumes to elevated CO2 (FACE) in a phosphorus-deficient vertisol

  • Jian Jin
  • Caixian Tang
  • Roger Armstrong
  • Peter Sale
Regular Article

Abstract

Background & aims

Understanding the mechanism of how phosphorus (P) regulates the response of legumes to elevated CO2 (eCO2) is important for developing P management strategies to cope with increasing atmospheric CO2 concentration. This study aimed to explore this mechanism by investigating interactive effects of CO2 and P supply on root morphology, nodulation and soil P fractions in the rhizosphere.

Methods

A column experiment was conducted under ambient (350 ppm) (aCO2) and eCO2 (550 ppm) in a free air CO2 enrichment (FACE) system. Chickpea and field pea were grown in a P-deficient Vertisol with P addition of 0–16 mg P kg−1.

Results

Increasing P supply increased plant growth and total P uptake with the increase being greater under eCO2 than under aCO2. Elevated CO2 increased root biomass and length, on average, by 16 % and 14 %, respectively. Nodule biomass increased by 46 % in response to eCO2 at 16 mg P kg−1, but was not affected by eCO2 at no P supply. Total P uptake was correlated with root length while N uptake correlated with nodule number and biomass regardless of CO2 level. Elevated CO2 increased the NaOH-extractable organic P by 92 % when 16 mg P kg−1 was applied.

Conclusion

The increase in P and N uptake and nodule number under eCO2 resulted from the increased biomass production, rather than from changes in specific root-absorbing capability or specific nodule function. Elevated CO2 appears to enhance P immobilization in the rhizosphere.

Keywords

Free air CO2 enrichment FACE N2 fixation Nodulation P acquisition P fractions Rhizosphere 

Notes

Acknowledgment

We thank Dr. Clayton Butterly and anonymous reviewers for reviewing the manuscript. This research was supported by an Australian Research Council Linkage Project (LP100200757), and utilised the SOILFACE facilities at DPI Horsham which were developed with funding by the Victorian Department of Primary Industries (VDPI), the University of Melbourne (UM), the Grains Research and Development Corporation (GRDC), the Federal Department of Agriculture, Fisheries and Forestry (DAFF) and the Australian Greenhouse Office (AGO).

References

  1. Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8PubMedCrossRefGoogle Scholar
  2. Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240CrossRefGoogle Scholar
  3. Ainsworth EA, Leakey ADB, Ort DR, Long SP (2008) FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2] impacts on crop yield and food supply. New Phytol 179:5–9PubMedCrossRefGoogle Scholar
  4. Barrett DJ, Richardson AE, Gifford RM (1998) Elevated atmospheric CO2 concentrations increase wheat root phosphatise activity when growth is limited by phosphorus. Aust J Plant Physiol 25:87–93CrossRefGoogle Scholar
  5. BassiriRad H, Reynolds JF, Virginia RA, Brunelle MH (1997) Growth and root NO3- and PO43- uptake capacity of three desert species in response to atmospheric CO2 enrichment. Aust J Plant Physiol 24:353–358CrossRefGoogle Scholar
  6. BassiriRad H, Gutschick VP, Lussenhop J (2001) Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126:305–320CrossRefGoogle Scholar
  7. Beck MA, Sanchez PA (1994) Soil-phosphorus fraction dynamics during 18 years of cultivation on a typic paleudult. Soil Sci Soc Am J 58:1424–1431CrossRefGoogle Scholar
  8. Berntson GM, Woodward FI (1992) The root-system architecture and development of Senecio vulgaris in elevated CO2 and drought. Funct Ecol 6:324–333CrossRefGoogle Scholar
  9. Bertrand A, Prevost D, Bigras FJ, Lalande R, Tremblay GF, Castonguay Y, Belanger G (2007) Alfalfa response to elevated atmospheric CO2 varies with the symbiotic rhizobial strain. Plant Soil 301:173–187CrossRefGoogle Scholar
  10. Binkley D, Giardina C, Bashkin MA (2000) Soil phosphorus pools and supply under the influence of Eucalyptus saligna and nitrogen-fixing Albizia facaltaria. For Ecol Manag 128:241–247CrossRefGoogle Scholar
  11. Bordeleau LM, Prevost D (1994) Nodulation and nitrogen-fixation in extreme environments. Plant Soil 161:115–125CrossRefGoogle Scholar
  12. Butterly CR, Buenemann EK, McNeill AM, Baldock JA, Marschner P (2009) Carbon pulses but not phosphorus pulses are related to decreases in microbial biomass during repeated drying and rewetting of soils. Soil Biol Biochem 41:1406–1416CrossRefGoogle Scholar
  13. Campbell CD, Sage RF (2002) Interactions between atmospheric CO2 concentration and phosphorus nutrition on the formation of proteoid roots in white lupin (Lupinus albus L.). Plant Cell Environ 25:1051–1059CrossRefGoogle Scholar
  14. Cassman KG, Whitney AS, Stockinger KR (1980) Root-growth and dry-matter distribution of soybean as affected by phosphorus stress, nodulation and nitrogen-source. Crop Sci 20:239–244CrossRefGoogle Scholar
  15. Cernusak LA, Winter K, Martinez C, Correa E, Aranda J, Garcia M, Jaramillo C, Turner BL (2011) Responses of legume versus non-legume tropical tree seedlings to elevated CO2 concentration. Plant Physiol 157:372–385PubMedCrossRefGoogle Scholar
  16. Colwell JD (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust J Exp Agric Anim Husb 3:190–198CrossRefGoogle Scholar
  17. Conroy JP, Milham PJ, Reed ML, Barlow EW (1990) Increases in phosphorus requirements for CO2-enriched pine species. Plant Physiol 92:977–982PubMedCrossRefGoogle Scholar
  18. Conroy JP, Milham PJ, Barlow EWR (1992) Effect of nitrogen and phosphorus availability on the growth-response of Eucalyptus grandis to high CO2. Plant Cell Environ 15:843–847CrossRefGoogle Scholar
  19. de Graaff MA, van Groenigen KJ, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Chang Biol 12:2077–2091CrossRefGoogle Scholar
  20. Erman M, Yildirim B, Togay N, Cig F (2009) Effect of phosphorus application and rhizobium inoculation on the yield, nodulation and nutrient uptake in field pea (Pisum sativum sp arvense L.). J Anim Vet Adv 8:301–304Google Scholar
  21. Fangmeier A, De Temmerman L, Mortensen L, Kemp K, Burke J, Mitchell R, van Oijen M, Weigel HJ (1999) Effects on nutrients and on grain quality in spring wheat crops grown under elevated CO2 concentrations and stress conditions in the European, multiple-site experiment ‘ESPACE-wheat’. Eur J Agron 10:215–229CrossRefGoogle Scholar
  22. FAO-UNESCO (1976) Soil map of the world, 1:5 000 000, vol. X, Australia. UNESCO, ParisGoogle Scholar
  23. Finn GA, Brun WA (1982) Effect of atmospheric CO2 enrichment on growth, non-structural carbohydrate content, and root nodule activity in soybean. Plant Physiol 69:327–331PubMedCrossRefGoogle Scholar
  24. Fitter AH, Self GK, Wolfenden J, vanVuuren MMI, Brown TK, Williamson L, Graves JD, Robinson D (1996) Root production and mortality under elevated atmospheric carbon dioxide. Plant Soil 187:299–306CrossRefGoogle Scholar
  25. Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320CrossRefGoogle Scholar
  26. Gates CT (1974) Nodule and plant development in Stylosanthes humilis H.B.K.: symbiotic response to phosphorus and sulphur. Aust J Bot 22:45–55CrossRefGoogle Scholar
  27. Gentile R, Dodd M, Lieffering M, Brock SC, Theobald PW, Newton PCD (2012) Effects of long-term exposure to enriched CO2 on the nutrient-supplying capacity of a grassland soil. Biol Fert Soil 48:357–362Google Scholar
  28. George TS, Gregory PJ, Wood M, Read D, Buresh RJ (2002) Phosphatase activity and organic acids in the rhizosphere of potential agroforestry species and maize. Soil Biol Biochem 34:1487–1494CrossRefGoogle Scholar
  29. Gerke J, Beissner L, Romer W (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. J Plant Nutr Soil Sci 163:207–212CrossRefGoogle Scholar
  30. Guppy CN, Menzies NW, Moody PW, Compton BL, Blamey FPC (2000) A simplified, sequential, phosphorus fractionation method. Commun Soil Sci Plant 31:1981–1991CrossRefGoogle Scholar
  31. Haase S, Neumann G, Kania A, Kuzyakov Y, Romheld V, Kandeler E (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221CrossRefGoogle Scholar
  32. Idso SB, Kimball BA, Mauney JR (1988) Effects of atmospheric CO2 enrichment on root-shoot ratios of carrot, radish, cotton and soybean. Agric Ecosyst Environ 21:293–299CrossRefGoogle Scholar
  33. Isbell RF (1996) The Australian soil classification. CSIRO Publishing, MelbourneGoogle Scholar
  34. Israel DW (1987) Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiol 84:835–840PubMedCrossRefGoogle Scholar
  35. Laby RJ, Kinkaid MS, Kim D, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23:587–596PubMedCrossRefGoogle Scholar
  36. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876PubMedCrossRefGoogle Scholar
  37. Lee TD, Tjoelker MG, Reich PB, Russelle MP (2003) Contrasting growth response of an N2-fixing and non-fixing forb to elevated CO2: dependence on soil N supply. Plant Soil 255:475–486CrossRefGoogle Scholar
  38. Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049PubMedCrossRefGoogle Scholar
  39. Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208CrossRefGoogle Scholar
  40. Mollah M, Partington D, Fitzgerald G (2011) Understand distribution of carbon dioxide to interpret crop growth data: Australian grains free-air carbon dioxide enrichment experiment. Crop Pasture Sci 62:883–891CrossRefGoogle Scholar
  41. Motomizu S, Wakimoto T, Toei K (1980) Spectrophotometric determination of phosphate in river waters with molybdite and malachite green. Analyst 108:361–367CrossRefGoogle Scholar
  42. Newbery RM, Wolfenden J, Mansfield TA, Harrison AF (1995) Nitrogen, phosphorus and potassium uptake and demand in Agrostis capillaris: the influence of elevated CO2 and nutrient supply. New Phytol 130:565–574CrossRefGoogle Scholar
  43. Niu Y, Jin C, Jin G, Zhou Q, Lin X, Tang C, Zhang Y (2011) Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh. under elevated CO2. Plant Cell Environ 34:1304–1317PubMedCrossRefGoogle Scholar
  44. Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2005) Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant Soil 271:175–187CrossRefGoogle Scholar
  45. 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
  46. Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2- enriched environments. New Phytol 147:55–71CrossRefGoogle Scholar
  47. Qiao YF, Tang CX, Han XZ, Miao SF (2007) Phosphorus deficiency delays the onset of nodule function in soybean. J Plant Nutr 30:1341–1353CrossRefGoogle Scholar
  48. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol 50:665–693CrossRefGoogle Scholar
  49. Raghothama KG, Muchhal US, Kim DH, Bucher M (1999) Molecular regulation of plant phosphate transporters. In: Lynch JP, Deikman J (eds) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes, American society of plant physiologists, Maryland pp 271–280Google Scholar
  50. Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods. Inkata Press, MelbourneGoogle Scholar
  51. Rennie RJ, Dubetz S (1986) Nitrogen-15-determined nitrogen fixation in field-grown chickpea, lentil, fababean, and field pea. Agron J 78:654–660CrossRefGoogle Scholar
  52. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  53. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996PubMedCrossRefGoogle Scholar
  54. Robson AD, O’Hara GW, Abbott LK (1981) Involvement of phosphorus in nitrogen-fixation by subterranean clover (Trifolium subterraneum L.). Aust J Plant Physiol 8:427–436CrossRefGoogle Scholar
  55. Rogers HH, Bingham GE, Cure JD, Smith JM, Surano KA (1983) Response of selected plant-species to elevated carbon-dioxide in the field. J Environ Qual 12:569–574CrossRefGoogle Scholar
  56. Rogers HH, Prior SA, Oneill EG (1992) Cotton root and rhizosphere responses to free-air CO2 enrichment. Crit Rev Plant Sci 11:251–263Google Scholar
  57. Rogers HH, Prior SA, Runion GB, Mitchell RJ (1996) Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248CrossRefGoogle Scholar
  58. Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016PubMedCrossRefGoogle Scholar
  59. Sa TM, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97:928–935PubMedCrossRefGoogle Scholar
  60. SAS (1997) SAS user’s guide: statistics. Version 6.12. SAS Institute, CaryGoogle Scholar
  61. Schortemeyer M, Atkin OK, McFarlane N, Evans JR (2002) N2 fixation by Acacia species increases under elevated atmospheric CO2. Plant Cell Environ 25:567–579CrossRefGoogle Scholar
  62. Sinclair TR (1992) Mineral nutrition and plant growth response to climate change. J Exp Bot 43:1141–1146CrossRefGoogle Scholar
  63. Srinivasarao C, Ganeshamurthy AN, Ali M, Venkateswarlu B (2006) Phosphorus and micronutrient nutrition of chickpea genotypes in a multi-nutrient-deficient typic ustochrept. J Plant Nutri 29:747–763CrossRefGoogle Scholar
  64. Srivastava AC, Pal M, Sengupta UK (2002) Changes in nitrogen metabolism of Vigna radiata in response to elevated CO2. Biol Plant 45:395–399CrossRefGoogle Scholar
  65. Steel RG, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  66. Stöcklin J, Körner C (1999) Interactive effects of elevated CO2, P availability and legume presence on calcareous grassland: results of a glasshouse experiment. Funct Ecol 13:200–209CrossRefGoogle Scholar
  67. Stöcklin J, Schweizer K, Körner C (1998) Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland. Oecologia 116:50–56CrossRefGoogle Scholar
  68. Tang C, Robson AD, Dilworth MJ (1990) A split-root experiment shows that iron is required for nodule initiation in Lupinus angustifolius L. New Phytol 115:61–67CrossRefGoogle Scholar
  69. Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environ Exp Bot 67:228–234CrossRefGoogle Scholar
  70. Turner BL, Condron LM, Richardson SJ, Peltzer DA, Allison VJ (2007) Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–1181CrossRefGoogle Scholar
  71. Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197CrossRefGoogle Scholar
  72. von Felten S, Hättenschwiler S, Saurer M, Siegwolf R (2007) Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees 21:283–294CrossRefGoogle Scholar
  73. Vu DT, Armstrong RD, Sale PWG, Tang C (2010) Phosphorus availability for three crop species as a function of soil type and fertilizer history. Plant Soil 337:497–510CrossRefGoogle Scholar
  74. West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric CO2. New Phytol 167:523–530PubMedCrossRefGoogle Scholar
  75. Whitehead SJ, Caporn SJM, Press MC (1997) Effects of elevated CO2, nitrogen and phosphorus on the growth and photosynthesis of two upland perennials: Calluna vulgaris and Pteridium aquilinum. New Phytol 135:201–211CrossRefGoogle Scholar
  76. Wolf J (1996) Effects of nutrient supply (NPK) on spring wheat response to elevated atmospheric CO2. Plant Soil 185:113–123CrossRefGoogle Scholar
  77. Wouterlood M, Lambers H, Veneklaas EJ (2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Funct Plant Biol 32:153–159CrossRefGoogle Scholar
  78. Yuen SH, Pollard AG (1954) Determination of nitrogen in agricultural materials by the Nessler Reagent. II. Micro-determination of plant tissue and soil extracts. J Sci Food Agric 5:364–369CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Jian Jin
    • 1
    • 3
  • Caixian Tang
    • 1
  • Roger Armstrong
    • 2
  • Peter Sale
    • 1
  1. 1.Department of Agricultural SciencesLa Trobe UniversityMelbourneAustralia
  2. 2.Department of Primary IndustriesPMB 260HorshamAustralia
  3. 3.Key Laboratory of Black Soil Ecology, Northeast Institute of Geography and Agroecology, Chinese Academy of SciencesHarbinChina

Personalised recommendations