Plant and Soil

, Volume 416, Issue 1–2, pp 283–295 | Cite as

Rhizosphere-driven increase in nitrogen and phosphorus availability under elevated atmospheric CO2 in a mature Eucalyptus woodland

  • Raúl Ochoa-Hueso
  • John Hughes
  • Manuel Delgado-Baquerizo
  • John E. Drake
  • Mark G. Tjoelker
  • Juan Piñeiro
  • Sally A. Power
Regular Article


Background and aims

Rhizosphere processes are integral to carbon sequestration by terrestrial ecosystems in response to rising concentrations of atmospheric CO2. Yet, the nature and magnitude of rhizosphere responses to elevated CO2, particularly in nutrient and water-limited forest ecosystems, remain poorly understood.


We investigated rhizosphere responses (enzyme activities and nutrient availability) to atmospheric CO2 enrichment (ambient +150 μmol CO2 mol−1) in a phosphorus-limited mature eucalypt woodland in south-eastern Australia (the EucFACE experiment).


Following 17 months of treatment, the activity of rhizosphere soil exoenzymes related to starch and cellulose degradation decreased between 0 and 10 cm and increased from 10 to 30 cm depth under elevated CO2. This response was concurrent with increases in nitrogen and phosphorus availability and smaller C:P nutrient ratios in rhizosphere soil under elevated CO2.


This nutrient-poor eucalypt woodland exhibited rhizosphere responses to atmospheric CO2 enrichment that increased nutrient availability in rhizosphere soil and suggest accelerated rates of soil organic matter decomposition, both of which may, in turn, promote plant growth under elevated CO2 concentrations.


Climate change Elevated CO2 Free-air CO2 enrichment Fine roots Forests Nutrient limitation Phosphorus Rhizosphere 



We are grateful to Prof. David Ellsworth, Burhan Amiji, Dr. Craig Barton, Dr. Vinod Kumar and Steven Wohl for managing the EucFACE facility. EucFACE is an initiative supported by the Australian Government through the Education Investment Fund, the Department of Industry and Science, and the Australian Research Council in partnership with the Western Sydney University. Facilities at EucFACE were built as an initiative of the Australian Government as part of the Nation-building Economic Stimulus Package. The authors declare no conflicts of interest.

Supplementary material

11104_2017_3212_MOESM1_ESM.docx (36 kb)
Table S1 (DOCX 36 kb)
11104_2017_3212_MOESM2_ESM.docx (25 kb)
Table S2 (DOCX 24 kb)
11104_2017_3212_MOESM3_ESM.docx (28 kb)
Table S3 (DOCX 28 kb)
11104_2017_3212_MOESM4_ESM.docx (25 kb)
Table S4 (DOCX 24 kb)
11104_2017_3212_MOESM5_ESM.docx (2.4 mb)
Suppl. Fig. 1 (DOCX 2492 kb)
11104_2017_3212_MOESM6_ESM.docx (25 kb)
Suppl. Fig. 2 (DOCX 25 kb)
11104_2017_3212_MOESM7_ESM.docx (49 kb)
Suppl. Fig. 3 (DOCX 49 kb)


  1. Adl S (2016) Rhizosphere, food security, and climate change: a critical role for plant-soil research. Rhizosphere 1:1–3. doi: 10.1016/j.rhisph.2016.08.005 CrossRefGoogle Scholar
  2. Allen AS, Andrews JA, Finzi AC et al (2000) Effects of free-air CO2 enrichment (FACE) on belowground processes in a Pinus taeda forest. Ecol Appl 10:437–448. doi: 10.1890/1051-0761(2000)010[0437:EOFACE]2.0.CO;2 Google Scholar
  3. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85(10):2682–2686. doi: 10.1890/03-0650 CrossRefGoogle Scholar
  4. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. doi: 10.1111/j.1365-3040.2009.01926.x CrossRefPubMedGoogle Scholar
  5. Bell CW, Fricks BE, Rocca JD et al (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities J Vis Exp:e50961. doi: 10.3791/50961
  6. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi: 10.1016/j.tplants.2012.04.001 CrossRefPubMedGoogle Scholar
  7. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13CrossRefPubMedGoogle Scholar
  8. Carol Adair E, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob Chang Biol 17:3546–3563CrossRefGoogle Scholar
  9. Carrillo Y, Dijkstra FA, Pendall E et al (2014) Plant rhizosphere influence on microbial C metabolism: the role of elevated CO2, N availability and root stoichiometry. Biogeochemistry 117:229–240. doi: 10.1007/s10533-014-9954-5 CrossRefGoogle Scholar
  10. Chantigny MH, Angers DA, Kaiser K, Kalbitz K (2006) Extraction and characterization of dissolved organic matter. In: Carter MR, Gregorich E (eds) Soil sampling and methods of analysis., Second ed. CRC Press, Boca Raton, p 617–635Google Scholar
  11. Covelo F, Rodríguez A, Gallardo A (2008) Spatial pattern and scale of leaf N and P resorption efficiency and proficiency in a Quercus robur population. Plant Soil 311:109–119. doi: 10.1007/s11104-008-9662-9 CrossRefGoogle Scholar
  12. Crous KY, Ósvaldsson A, Ellsworth DS (2015) Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant Soil 391:293–305. doi: 10.1007/s11104-015-2426-4 CrossRefGoogle Scholar
  13. Day FP, Schroeder RE, Stover DB et al (2013) The effects of 11 yr of CO2 enrichment on roots in a Florida Scrub-oak ecosystem. New Phytol 200:778–787. doi: 10.1111/nph.12246 CrossRefPubMedGoogle Scholar
  14. de Graaff M-A, van Groenigen K-J, Six J et al (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Chang Biol 12:2077–2091. doi: 10.1111/j.1365-2486.2006.01240.x CrossRefGoogle Scholar
  15. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:1–8. doi: 10.3389/fmicb.2013.00216 CrossRefGoogle Scholar
  16. Drake JE, Darby BA, Giasson M-A et al (2013) Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838. doi: 10.5194/bg-10-821-2013 CrossRefGoogle Scholar
  17. Drake JE, Gallet-Budynek A, Hofmockel KS et al (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357. doi: 10.1111/j.1461-0248.2011.01593.x CrossRefPubMedGoogle Scholar
  18. Drake JE, Macdonald C, Tjoelker MG et al (2016) Short-term carbon cycling responses of a mature eucalypt woodland to gradual stepwise enrichment of atmospheric CO2 concentration. Glob Chang Biol 22:380–390. doi: 10.1111/gcb.13109 CrossRefPubMedGoogle Scholar
  19. Finzi AC, Abramoff RZ, Spiller KS et al (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094. doi: 10.1111/gcb.12816 CrossRefPubMedGoogle Scholar
  20. Finzi AC, Sinsabaugh RL, Long TM, Osgood MP (2006) Microbial community responses to atmospheric carbon dioxide enrichment in a warm-temperate forest. Ecosystems 9:215–226. doi: 10.1007/s10021-005-0078-6 CrossRefGoogle Scholar
  21. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi: 10.1016/S0038-0717(03)00123-8 CrossRefGoogle Scholar
  22. Friend AD, Lucht W, Rademacher TT et al (2014) Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2. Proc Natl Acad Sci U S A 111:3280–3285. doi: 10.1073/pnas.1222477110 CrossRefPubMedGoogle Scholar
  23. Gimeno TE, Crous KY, Cooke J et al (2015) Conserved stomatal behaviour under elevated CO2 and varying water availability in a mature woodland. Funct Ecol 30:700–709. doi: 10.1111/1365-2435.12532 CrossRefGoogle Scholar
  24. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14. doi: 10.1007/s11104-007-9514-z CrossRefGoogle Scholar
  25. Hasegawa S, Macdonald CA, Power SA (2016) Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited eucalyptus woodland. Glob Chang Biol 22:1628–1643. doi: 10.1111/gcb.13147 CrossRefPubMedGoogle Scholar
  26. Hinsinger P, Bengough a. G, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. doi:  10.1007/s11104-008-9885-9
  27. Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357. doi: 10.1111/j.1469-8137.2009.03122.x CrossRefPubMedGoogle Scholar
  28. Jin J, Tang C, Sale P (2015) The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review. Ann Bot doi:  10.1093/aob/mcv088
  29. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33. doi: 10.1007/s11104-009-9925-0 CrossRefGoogle Scholar
  30. Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31. doi: 10.1016/j.pbi.2015.04.002 CrossRefPubMedGoogle Scholar
  31. Liberloo M, Tulva I, Raïm O et al (2007) Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytol 173:537–549. doi: 10.1111/j.1469-8137.2006.01926.x CrossRefPubMedGoogle Scholar
  32. Macinnis-Ng CMO, Fuentes S, O’Grady AP et al (2009) Root biomass distribution and soil properties of an open woodland on a duplex soil. Plant Soil 327:377–388. doi: 10.1007/s11104-009-0061-7 CrossRefGoogle Scholar
  33. Matamala R, Schlesinger WH (2000) Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem. Glob Chang Biol 6:967–979. doi: 10.1046/j.1365-2486.2000.00374.x CrossRefGoogle Scholar
  34. McCarthy HR, Oren R, Johnsen KH et al (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol 185:514–528. doi: 10.1111/j.1469-8137.2009.03078.x CrossRefPubMedGoogle Scholar
  35. Nguyen C (2009) Rhizodeposition of organic C by plants: mechanisms and controls. In: Navarrete M, Debaeke P et al (eds) Eric Lichtfouse. Sustainable Agriculture, Springer Netherlands, pp 97–123Google Scholar
  36. Nie M, Lu M, Bell J et al (2013) Altered root traits due to elevated CO2: a meta-analysis. Glob Ecol Biogeogr 22:1095–1105. doi: 10.1111/geb.12062 CrossRefGoogle Scholar
  37. Norby RJ, De Kauwe MG, Domingues TF et al (2015) Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. New Phytol 209:17–28. doi: 10.1111/nph.13593 CrossRefPubMedGoogle Scholar
  38. Palmroth S, Oren R, McCarthy HR et al (2006) Aboveground sink strength in forests controls the allocation of carbon below ground and its [CO2]-induced enhancement. Proc Natl Acad Sci U S A 103:19362–19367. doi: 10.1073/pnas.0609492103 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799CrossRefPubMedGoogle Scholar
  40. Phillips RP, Fahey TJ (2005) Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings. Glob Chang Biol 11:983–995. doi: 10.1111/j.1365-2486.2005.00959.x CrossRefGoogle Scholar
  41. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. doi: 10.1111/j.1461-0248.2010.01570.x CrossRefPubMedGoogle Scholar
  42. Phillips RP, Meier IC, Bernhardt ES et al (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15:1042–1049. doi: 10.1111/j.1461-0248.2012.01827.x CrossRefPubMedGoogle Scholar
  43. Pritchard SG, Strand AE, McCormack ML et al (2008) Fine root dynamics in a loblolly pine forest are influenced by free-air-CO2 -enrichment: a six-year-minirhizotron study. Glob Chang Biol 14:588–602. doi: 10.1111/j.1365-2486.2007.01523.x CrossRefGoogle Scholar
  44. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Rayment G, Lyons D (2011) Soil chemical methods - Australasia. CSIRO Publishing, Collingwood, VictoriaGoogle Scholar
  46. Sinsabaugh RL, Belnap J, Rudgers J et al (2015) Soil microbial responses to nitrogen addition in arid ecosystems. Front Microbiol 6:819. doi: 10.3389/fmicb.2015.00819 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. doi: 10.1038/nature08632 CrossRefPubMedGoogle Scholar
  48. Stover DB, Day FP, Butnor JR, Drake BG (2007) Effect of elevated CO2 on coarse-root biomass in Florida Scrub detected by ground-penetrating radar. Ecology 88:1328–1334. doi: 10.1890/06-0989 CrossRefPubMedGoogle Scholar
  49. Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411. doi: 10.1890/1051-0761(2000)010[0399:AOSOMA]2.0.CO;2 CrossRefGoogle Scholar
  50. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15Google Scholar
  51. Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282. doi: 10.5194/bg-7-2261-2010 CrossRefGoogle Scholar
  52. Zak DR, Pregitzer KS, Curtis PS, Holmes WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10:47–59. doi: 10.1890/1051-0761(2000)010[0047:ACATCA]2.0.CO;2 Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  2. 2.Department of EcologyAutonomous University of MadridMadridSpain
  3. 3.School of GeographyUniversity of LeedsLeedsUK
  4. 4.Cooperative Institute for Research in Environmental SciencesUniversity of ColoradoBoulderUSA

Personalised recommendations