Plant and Soil

, Volume 187, Issue 2, pp 277–288 | Cite as

Influence of rhizodeposition under elevated CO2 on plant nutrition and soil organic matter

  • Zoe G. Cardon
Carbon Allocation Mechanisms and Controls Direct Carbon Losses from Roots


Atmospheric CO2 concentrations can influence ecosystem carbon storage through net primary production (NPP), soil carbon storage, or both. In assessing the potential for carbon storage in terrestrial ecosystems under elevated CO2, both NPP and processing of soil organic matter (SOM), as well as the multiple links between them, must be examined. Within this context, both the quantity and quality of carbon flux from roots to soil are important, since roots produce specialized compounds that enhance nutrient acquisition (affecting NPP), and since the flux of organic compounds from roots to soil fuels soil microbial activity (affecting processing of SOM).

From the perspective of root physiology, a technique is described which uses genetically engineered bacteria to detect the distribution and amount of flux of particular compounds from single roots to non-sterile soils. Other experiments from several labs are noted which explore effects of elevated CO2 on root acid phosphatase, phosphomonoesterase, and citrate production, all associated with phosphorus nutrition. From a soil perspective, effects of elevated CO2 on the processing of SOM developed under a C4 grassland but planted with C3 California grassland species were examined under low (unamended) and high (amended with 20 g m−2 NPK) nutrients; measurements of soil atmosphere δ13C combined with soil respiration rates show that during vegetative growth in February, elevated CO2 decreased respiration of carbon from C4 SOM in high nutrient soils but not in unamended soils.

This emphasis on the impacts of carbon loss from roots on both NPP and SOM processing will be essential to understanding terrestrial ecosystem carbon storage under changing atmospheric CO2 concentrations.

Key words

carbon isotopes carbon storage elevated CO2 phosphorus rhizodeposition root exudation soil organic matter 



soil organic matter


net primary productivity


net ecosystem productivity


p-nitrophenyl phosphate


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Attiwell, P M and Leeper, G M 1987 Forest soils and nutrient cycles. Melbourne University Press, Melbourne, Australia.Google Scholar
  2. Balesdent, J, Mariotti, A and Guillet, B 1987 Natural 13C abundance as a tracer for studies of soil organic matter dynamics. Soil Biol. Biochem. 19, 25–30.Google Scholar
  3. Barber, D A and Martin, J K 1976 The release of organic substances by cereal roots into soil. New Phytol. 76, 69–80.Google Scholar
  4. Barber, S A 1984 Soil Nutrient Bioavailability. Wiley Interscience, NY, USA.Google Scholar
  5. Bauer, W D and Caetano-Anolles, G 1990 Chemotaxis, induced gene expression and competitiveness in the rhizosphere. Plant and Soil 129, 45–52.Google Scholar
  6. Bazzaz, F A 1990 The response of natural ecosystems to the rising global CO2 levels. Annu. Rev. Ecol. Syst. 21, 167–196.CrossRefGoogle Scholar
  7. Blair, N, Leu, A, Munoz, E, Olsen, J, Kwong, E and Des Marais, D 1985 Carbon isotopic fractionation in heterotrophic microbial metabolism. Appl. Environ. Microbiol. 50,9 96–1001.Google Scholar
  8. Bowes, G 1993 Facing the inevitable: plants and increasing atmospheric CO2. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 309–332.CrossRefGoogle Scholar
  9. Buol, F, Hole, F and McCracken, R 1980 Soil Genesis and Classification. Iowa State University Press, Ames, USA. 243 p.Google Scholar
  10. Cardon, Z G and Jackson, R B 1995 The Jasper Ridge elevated CO2 experiment: root acid phosphatase activity in Bromus hordeaceus and Avena barbata remains unchanged under elevated CO2. Bull. Ecol. Soc. Am. 76 (2 Suppl. Part 2), 39–40.Google Scholar
  11. Cardon Z G, Hungate B A, Chapin III F S, Field CB and Holland E A 1996 Effects of soil nutrient availability on processing of SOM under elevated CO2. Bull. Ecol. Soc. Am. 77 Suppl, 70.Google Scholar
  12. Cerling, T E, Solomon, D K, Quade, J and Bowman, J R 1991 On the isotopic composition of carbon in soil carbon dioxide. Geochim. Cosmochim. Acta 55, 3403–3405.CrossRefGoogle Scholar
  13. Ceulemans, R and Mousseau, M 1994 Tansley Review No. 71 Effects of elevated atmospheric CO2 on woody plants. New Phytol. 127, 425–446.Google Scholar
  14. ChapinIII, F S 1980 The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233–260.CrossRefGoogle Scholar
  15. Clarholm, M 1985 Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17, 181–187.CrossRefGoogle Scholar
  16. Clark, E, Brandl, M and Lindow, S E 1992 Aromatic aminotransferase genes from an indoleacetic acid-producing Erwinia herbicola strain. Phytopathology 82, 1100.Google Scholar
  17. Cotrufo, M F, Ineson, P and Rowland, A P 1994 Decomposition of tree leaf litters grown under elevated CO2: Effect of litter quality. Plant and Soil 163, 121–130.Google Scholar
  18. Coteaûx, M-M, Mousseau, M, Celerier, M-L and Bottner, P 1991 Increased atmospheric CO2 and litter quality: decomposition of sweet chestnut leaf litter with animal food webs of different complexities. Oikos 61, 54–64.Google Scholar
  19. Dagley, S 1974 Citrate: UV spectrophotometric determination. In Methods of Enzymatic Analysis. Volume 3. Ed H UBergmeyer. pp 1562–1565. Academic Press, New York, USA.Google Scholar
  20. Diaz, S A, Grime, J P, Harris, J and McPherson, E 1993 Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. Nature 364, 616–617.CrossRefGoogle Scholar
  21. Dormaar, J F 1990 Effect of active roots on the decomposition of soil organic materials. Biol. Fertil. Soils 10, 121–126.Google Scholar
  22. Field, C B, ChapinIII, P S, Matson, P A and Mooney, H A 1992 Responses of terrestrial ecosystems to the changing atmosphere: a resource-based approach. Annu. Rev. Ecol. Syst. 23, 201–235.CrossRefGoogle Scholar
  23. Field, C B, ChapinIII, F S, Chiariello, N R, Holland, E A and Mooney, H A 1996 The Jasper Ridge CO2 experiment: design and motivation. In Carbon Dioxide and Terrestrial Ecosystems. Eds. G WKoch and H AMooney. pp 121–145. Academic Press, San Diego, USA.Google Scholar
  24. Garnier, E 1991 Resource capture, biomass allocation and growth in herbaceous plants. Trends Ecol. Evol. 6, 126–131.CrossRefGoogle Scholar
  25. Gifford R M, Lutze J L and Barrett D 1996 Global atmospheric change effects on terrestrial carbon sequestration: Exploration with a global C- and N-cycle model (CQUESTN). Plant and Soil 187.Google Scholar
  26. Harrison, K G, Post, W M and Richter, D D 1995 Soil carbon turnover in a recovering temperate forest. Global Biogeochem. Cyc. 9, 449–454.CrossRefGoogle Scholar
  27. Hoffland, E, Van denBoogaard, R, Nelemans, J A and Findenegg, G R 1992 Biosynthesis and root exudation of citric and malic acid in phosphate-starved rape plants. New Phytol. 122, 675–680.Google Scholar
  28. Hungate B A and Chapin III F S 1995 Terrestrial ecosystem response to elevated CO2: effects on microbial N transformations across gradients of nutrient availability. GCTE Focus 1 Workshop. Lake Tahoe, California, USA.Google Scholar
  29. Hungate B A, Chapin III F S, Zhong H, Holland E A and Field C B 1996a Stimulation of grassland nitrogen cycling under carbon dioxide enrichment. Oecologia (In press).Google Scholar
  30. Hungate B A, Jackson R B, Field C B and Chapin III F S 1996b Detecting changes in soil carbon in CO2 enrichment experiments. Plant and Soil 187.Google Scholar
  31. Ineson P, Cotrufo M F, Bol R, Harkness D D and Blum H 1996 Quantification of soil carbon inputs under elevated CO2: C3 plants in a C4 soil. Plant and Soil 187.Google Scholar
  32. Jackson, R B, Luo, Y, Cardon, Z G, Chiariello, N R, Sala, O E, Field, C B and Mooney, H A 1995 Photosynthesis, growth, and density for the dominant species in a CO2-enriched grassland. J Biogeog. 22, 221–225.Google Scholar
  33. Jackson, R B and Reynolds, H R 1995 Nitrate and ammonium uptake for single and mixed-species communities grown at elevated CO2. Oecologia 105, 74–80.CrossRefGoogle Scholar
  34. Jaeger, C HIII, Lindow, S E, ChapinIII, F S and Firestone, M K 1996 Interaction of roots and soil microorganisms in rhizosphere N cycling. Bull. Ecol. Soc. Am. 77 (Suppl), 215.Google Scholar
  35. Jones, D L and Darrah, P R 1993 Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere. II. Experimental and model evidence of simultaneous exudation and re-sorption of soluble C compounds. Plant and Soil 153, 47–59.Google Scholar
  36. Kemp, P R, Waldecker, D G, Owensby, C E and Reynolds, J F 1994 Effects of elevated CO2 and nitrogen fertilization pretreatments on decomposition of tallgrass prairie leaf litter. Plant and Soil 165, 115–127.Google Scholar
  37. Kochain, L B 1995 Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237–60.CrossRefGoogle Scholar
  38. Korner, C and Arnone, J A 1992 Responses to elevated carbon dioxide in artificial tropical ecosystems. Science 257, 1672–1675.Google Scholar
  39. Kroehler, C J and Linkins, A E 1988 The root surface phosphatases of Eriophorum vaginatum: Effects of temperature, pH, substrate concentration and inorganic phosphorus. Plant and Soil 105, 3–10.Google Scholar
  40. Leavitt, S W 1994 Carbon isotope dynamics of free-air CO2-enriched cotton and soils Agric. For. Meteorol. 70, 87–101.CrossRefGoogle Scholar
  41. Lekkerkerk, L J A, Van deGeijn, S C and VanVeen, J A 1990 Effects of elevated atmospheric CO2 levels on the carbon economy of a soil planted with wheat. In Soils and the Greenhouse Effect. Ed. A FBouwman. pp 423–429. John Wiley and Sons, Chichester, UKGoogle Scholar
  42. Liljeroth, E, VanVeen, J A and Miller, H J 1990 Assimilate translocation to the rhizosphere of two wheat lines and subsequent utilization by rhizosphere microorganisms at two soil nitrogen concentrations. Soil Biol. Biochem. 22, 1015–1021.CrossRefGoogle Scholar
  43. Liljeroth, E, Kuikman, P and VanVeen, J A 1994 Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant and Soil 151, 233–240.Google Scholar
  44. Lindgren, P B, Frederick, R, Govindarajan, A G, Panopoulos, N J, Staskawica, B J and Lindow, S E 1989 An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syringae pv. phaseolicola. EMBO J. 8, 1291–1301.PubMedGoogle Scholar
  45. Lindow, S E 1990 Bacterial ice-nucleation activity. In Methods in Phytobacteriology. Eds. ZKlement, KRudolph and D CSands. pp 428–434 Akadémiai Kiadó, Budapest, Hungary.Google Scholar
  46. Lindow, S E 1995 The use of reporter genes in the study of microbial ecology. Mol. Ecol. 4, 555–566.Google Scholar
  47. Loper, J E and Lindow, S E 1994 A biological sensor for iron available to bacteria in their habitats on plant surfaces. Appl. Environ. Microbiol. 60, 1934–1941.Google Scholar
  48. Lynch, J M and Whipps, J M 1990 Substrate flow in the rhizosphere. Plant and Soil 129, 1–10.Google Scholar
  49. Marschner, H 1995 Mineral Nutrition of Higher Plants. 2nd edition. Academic Press, San Diego, USA.Google Scholar
  50. Mary, B, Mariotti, A and Morel, J L 1992 Use of 13C variations at natural abundance for studying the biodegradation of root mucilage, roots and glucose in soil. Soil Biol. Biochem. 24, 1065–1072.CrossRefGoogle Scholar
  51. Merckx, R, Dijkstra, A, denHartog, A and VanVeen, J A 1987 Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol. Fertil. Soils 5, 126–132.CrossRefGoogle Scholar
  52. Mott, K A 1988 Do stomata respond to carbon dioxide concentrations other than intercellular? Plant Physiol. 86, 200–203.Google Scholar
  53. Norby, R J 1994 Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant and Soil 165, 9–20.Google Scholar
  54. Norby, R J, O'Neill, E G, Hood, W G and Luxmoore, R J 1987 Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment. Tree Physiol. 3, 203–210.PubMedGoogle Scholar
  55. Oades, J M 1988 The retention of organic matter in soils. Biogeochem. 5, 35–70.Google Scholar
  56. O'Neill, E G 1994 Responses of soil biota to elevated atmospheric carbon dioxide. Plant and Soil 165, 55–65.Google Scholar
  57. Rice, C W, Garcia, F O, Hampton, C O and Owensby, C E 1994 Soil microbial response in tallgrass prairie to elevated CO2. Plant and Soil 165, 67–74.Google Scholar
  58. Robinson, D, Griffiths, B, Ritz, K and Wheatley, R 1989 Root-induced nitrogen mineralisation: A theoretical analysis. Plant and Soil 117, 185–193.Google Scholar
  59. Rogers, H H, Runion, G C and Krupa, S V 1994 Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ. Pollut. 83, 155–189.CrossRefPubMedGoogle Scholar
  60. Römheld, A 1991 The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: An ecological approach. Plant and Soil 130, 127–134.Google Scholar
  61. Sanchez, P 1976 Properties and Management of Soils in the Tropics. Wiley and Son, NY, USA. pp 254–295.Google Scholar
  62. Schonwitz, R, Stichler, W and Ziegler, H 1986 d 13C values of CO2 from soil respiration on sites with crops of C3 and C4 type of photosynthesis. Oecologia 69, 305–308.Google Scholar
  63. Silberbush, M, Homer-Ilan, A and Waisel, Y 1981 Root surface phosphatase activity in ecotypes of Aegilops peregrina. Physiol. Plant. 53, 501–504.Google Scholar
  64. Stulen, I and denHertog, J 1993 Root growth and functioning under atmospheric CO2 enrichment. Vegetatic 104/105, 99–115.Google Scholar
  65. Swinnen, J, VanVeen, J A and Merckx, R 1994 14C pulse-labelling of field-grown spring wheat: an evaluation of its use in rhizosphere carbon budget estimations. Soil Biol. Biochem. 26, 161–170.CrossRefGoogle Scholar
  66. Tarafdar, J C and Jungk, A 1987 Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol. Fertil. Soils 3, 199–204.Google Scholar
  67. Treeby, M, Marschner, H and Römheld, V 1989 Mobilization of iron and other micronutrients from a calcareous soil by plant-borne, microbial, and synthetic metal chelators. Plant and Soil 114, 217–226.Google Scholar
  68. Van deGeijn, S C and VanVeen, J A 1993 Implications of increased carbon dioxide levels for carbon input and turnover in soils. Vegetatio 104/105, 283–292.Google Scholar
  69. VanVeen, J A, Merckx, R and Van deGeijn, S C 1989 Plant and soil related controls of the flow of carbon from roots through the soil microbial biomass. Plant and Soil 115, 179–188.Google Scholar
  70. VanVeen, J A and Kuikman, P J 1990 Soil structural aspects of decomposition of organic matter by micro-organisms. Biogeochem. 11, 213–233.Google Scholar
  71. VanVeen, J A, Liljeroth, E, Lekkerkerk, L J A and Van deGeijn, S C 1991 Carbon fluxes in plant-soil systems at elevated atmospheric CO2 levels. Ecol. Appl. 1, 175–181.Google Scholar
  72. Vitousek, P M and Sanford, R LJr 1986 Nutrient cycling in moist tropical forest. Annu. Rev. Ecol. Syst. 17, 137–167.CrossRefGoogle Scholar
  73. Warembourg, F R and Paul, E A 1973 The use of 14CO2 canopy techniques for measuring carbon transfer through the plant-soil system. Plant and Soil 38, 331–345.Google Scholar
  74. Whipps, J M 1985 Effect of CO2 concentration on growth, carbon distribution and loss of carbon from the roots of maize. J. Exp. Bot. 36, 644–651.Google Scholar
  75. Whipps, J M 1990 Carbon economy. In The Rhizosphere. Ed. J MLynch. pp 59–97. John Wiley and Sons, Chichester, UK.Google Scholar
  76. Wood, C W, Torbert, H A, Rogers, H H, Runion, G B and Prior, S A 1994 Free-air CO2 enrichment effects on soil carbon and nitrogen. Agric. For. Meteorol. 70, 103–116.CrossRefGoogle Scholar
  77. Zak, D R, Pregitzer, K S, Curtis, P S, Teeri, J A, Fogel, R and Randlett, D L 1993 Elevated atrnospheric CO2 and feedback between carbon and nitrogen cycles. Plant and Soil 151, 105–117.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Zoe G. Cardon
    • 1
  1. 1.Department of Integrative Biology, Valley Life Sciences BuildingUniversity of CaliforniaBerkeleyUSA

Personalised recommendations