Skip to main content
Log in

Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Cadmium (Cd) accumulation has been found to vary between cultivars of durum wheat (Triticum turgidum var. durum), and it is hypothesized that low-molecular-weight organic acids (LMWOAs) produced at the soil-root interface (rhizosphere) may play an important role in the availability and uptake of Cd by these plants. The objective of this study, therefore, was to (1) investigate the nature and quantity of LMWOAs present in the rhizosphere of durum wheat cultivars Arcola (low Cd accumulator) and Kyle (high Cd accumulator) grown in three different soils: Yorkton, Sutherland and Waitville, and (2) determine the relationship between Cd accumulation in these plants and LMWOAs present in the rhizosphere. Plants were grown for two weeks in pot-cultures under growth chamber conditions. Oxalic, fumaric, succinic, L-malic, tartaric, citric, acetic, propionic and butyric acids were found and quantified in the water extracts of rhizosphere soil, with acetic and succinic acids being predominant. No water extractable LMWOAs were identified in the bulk soil. Total amount of LMWOAs in the rhizosphere soil of the high Cd accumulator (Kyle) was significantly higher than that for the low Cd accumulator (Arcola) in all three soils. Furthermore, large differences in amounts of LMWOAs were found in the rhizosphere soil for the same cultivars grown in different soils and followed the pattern: Sutherland > Waitville > Yorkton. Extractable soil Cd (M NH4Cl) and Cd accumulation in the plants also followed the same soil sequence as LMWOA production. Cadmium accumulation by the high and low Cd accumulating cultivars was proportional to the levels of LMWOAs found in the rhizosphere soil of each cultivar. These results suggest that the differing levels of LMWOAs present in the rhizosphere soil played an important role in the solubilization of particulate-bound Cd into soil solution and its subsequent phytoaccumulation by the high and low Cd accumulating cultivars.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barber D A and Martin J K 1976 The release of organic substances by cereal roots into soil. New Pathol. 76, 69–80.

    Google Scholar 

  • Basu U, Douglas G and Taylor G J 1994 Aluminum resistance in Triticum aestivum associated with enhanced exudation of malate. J. Plant Physiol. 144, 747–753.

    Google Scholar 

  • Baziramakenga R, Simard R R and Leroux G D 1995 Determination of organic acids in soil extracts by ion chromatography. Soil Biol. Biochem. 27, 349–356.

    Google Scholar 

  • Cieśliński G, Neilsen G H and Hogue E J 1995 Effect of pH and Cd concentration on Cd accumulation by apple trees (Malus domestica Borkh) cv. Fuji. Proc. 2nd International Symposium on Diagnosis of Nutritional Status of Deciduous Fruit Orchards, Trento, Italy, September 1993.

  • Cieśliński G, Van Rees K C J, Huang P M, Kozak L M, Rostad H P W and Knott D R 1996 Cadmium uptake and bioaccumulation in selected cultivars of durum wheat and flax as affected by soil type. Plant Soil 182, 115–124.

    Google Scholar 

  • Cieśliński G, Van Rees K C J, Szmigielska A M and Huang P M 1997 Low molecular weight organic acids released from roots of durum wheat and flax into the sterile nutrient solution. J. Plant Nutr. 20, 753–764.

    Google Scholar 

  • Cottenie A, Verloo M, Kiekens L, Camerlynck R, Velghe G and Dhaese A 1983 Essential and nonessential trace elements in the system soil-water-plant. Lab. Analyt. Agrochem. State Univ., Ghent, Belgium. 75 p.

    Google Scholar 

  • Cromack K Jr, Sollins P, Graustein W C, Speidel K, Todd A W, Spycher G, Li C Y and Todd R L 1979 Calcium oxalate accumulation in soil weathering and its mats of the hypogeous fungus Hysterangium crassum. Soil Biol. Biochem. 14, 463–468.

    Google Scholar 

  • Cutler J M and Rains D W 1974 Characterization of cadmium uptake by plant tissue. Plant Physiol. 54, 67–71.

    Google Scholar 

  • Elgala A M and Amberger A 1988 Root exudate and the ability of corn to utilize insoluble sources of iron. J. Plant Nutr. 11, 677–690.

    Google Scholar 

  • Florijn P J and Van Beusichem M L 1993 Uptake and distribution of cadmium in maize inbred lines. Plant Soil 150, 25–32.

    Google Scholar 

  • Fox T R and Comerford N B 1990 Low molecular weight organic acids in selected forest soils of the Southwestern USA. Soil Sci. Soc. Amer. J. 54, 1139–1144.

    Google Scholar 

  • Galal-Gorchev H 1993 Dietary intake, levels in food and estimated intake of lead, cadmium, and mercury. Food Addit. Contam. 10, 115–128.

    Google Scholar 

  • Jones D L, Darrah P R and Kochian L V 1996 Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180, 57–66.

    Google Scholar 

  • Jones J B and Case V W 1990 Sampling, handling and analyzing plant tissue samples. In: Soil Testing and Plant Analysis. 3rd edn. Ed. R L Westerman. pp 389–427. SSSA, Madison, WI, USA.

    Google Scholar 

  • Kabata-Pendias A and Pendias H 1992 Trace Elements in Soils and Plants. 2nd edn. CRC Press Inc., Boca Raton, FL, USA. 365 p.

    Google Scholar 

  • Kafkafi U, Welch R M, Norvell W A, Zasoski R J and Baligar V C 1992 Assessment of current knowledge concerning the chemistry and biology of root-soil interface. J. Plant Nutr. 15, xix-xxii.

    Google Scholar 

  • Kloss M, Iwannek K-H, Fendrik I and Nieman E G 1984 Organic acids in the root exudates of Diplachne fusca (Linn.) Beauv. Envir. Exp. Bot. 24, 179–188.

    Google Scholar 

  • Kraffczyk I, Trolldenier G and Beringer H 1984 Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol. Biochem. 16, 315–322.

    Google Scholar 

  • Krishnamurti G S R and Huang P M 1987 Influence of constituents on the stability of mechanical separates of soils representing major taxonomic orders. Appl. Clay Sci. 2, 299–308.

    Google Scholar 

  • Krishnamurti G S R, Huang P M, Van Rees K C J, Kozak L M and Rostad H P W 1994 Microwave digestion for detection of total cadmium in soils. Comm. Soil Sci. Plant Anal. 25, 615–625.

    Google Scholar 

  • Krishnamurti G S R, Huang P M, Van Rees K C J, Kozak L M and Rostad H P W 1995a A new soil test for the determination of plant-available cadmium in soils. Commun. Soil Sci. Plant Anal. 26, 2857–2867.

    Google Scholar 

  • Krishnamurti G S R, Huang P M, Van Rees K C J, Kozak L M and Rostad H P W 1995b Speciation of particulate-bound cadmium of soils and its bioavailability. The Analyst 120, 659–665.

    Google Scholar 

  • Krishnamurti G S R, Cieśliński G, Huang P M and Van Rees K C J 1997 Kinetics of cadmium release from soils as influenced by organic acids: Implication in cadmium availability. J. Environ. Qual. 26: 271–277.

    Google Scholar 

  • Krotz R M, Evangelou B P and Wagner G J 1989 Relationship between cadmium, zinc, Cd-peptide, and organic acids in tobacco suspension cells. Plant Physiol. 91, 780–787.

    Google Scholar 

  • Lilienholm B C, Dudley L M and Juriniak J J 1992 Oxalate determination in soils using ion chromatography. Soil Sci. Soc. Amer. J. 56, 324–326.

    Google Scholar 

  • Marschner H 1995 Mineral Nutrition of Higher Plants. 2nd edn. Academic Press, San Diego, CA, USA.

    Google Scholar 

  • Marschner H, Treeby M and Romheld V 1989 Role of root-induced changes in the rhizosphere for iron acquisition in higher plants. Z. Pflanzenernahr. Bodenk. 152, 197–204.

    Google Scholar 

  • McKeague J A 1978 Manual of sampling and methods analysis. Can. Soc. Soil Sci., Ottawa, Canada. 212 p.

  • Mench M and Martin E 1991 Mobilization of cadmium and other metals from two soils by root exudates of Zea mays L., Nicotiana tabacum L., and Nicotiana rustica L. Plant Soil 132, 187–196.

    Google Scholar 

  • Mench M, Morel J L, Guckert A and Gruillet B 1988 Metal binding with root exudates of low molecular weight. J. Soil Sci. 39, 521–527.

    Google Scholar 

  • Mitchell G A, Bingham F T, and Page A L 1978 Yield and metal composition of lettuce and wheat grown on soils amended with sewage sludge enriched with cadmium, copper, nickel, and zinc. J. Environ. Qual. 7, 165–171.

    Google Scholar 

  • Pellet D M, Grunes D L and Kochian L V 1995 Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196, 788–795.

    Google Scholar 

  • Petersen W and Bottger M 1991 Contribution of organic acids to the acidification of the rhizosphere of maize seedlings. Plant Soil 132, 152–163.

    Google Scholar 

  • Rovira A D 1969 Plant root exudates. Bot. Rev. 35, 35–57.

    Google Scholar 

  • Rovira A D and McDougall B 1967 Microbiological and biochemical aspects of the rhizosphere. In Soil Biochemistry. Eds. A D McLaren and G F Peterson. pp 417–463. Marcel Dekker, New York.

    Google Scholar 

  • Ryan P R, Delhaize E and Randall P J 1995 Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust. J. Plant Physiol. 22, 531–536.

    Google Scholar 

  • Smith R M and Martell A E 1976 Critical Stability Constants. Vol. 4. Inorganic Complexes. Plenum Press, New York, USA.

    Google Scholar 

  • Smith R M and Martell A E 1977 Critical Stability Constants. Vol. 3. Other Organic Ligands. Plenum Press, New York, USA.

    Google Scholar 

  • Soltanpour P N 1991 Determination of nutrient availability and elemental toxicity by ABDTPA soil test and ICPS. Adv. Soil. Sci. 16, 165–190.

    Google Scholar 

  • Stevenson F J 1967 Organic acids in soil. In Soil Biochemistry, Vol. 1. Eds. A D McLaren and G H Peterson. pp 119–149. Marcel Dekker, New York, USA.

    Google Scholar 

  • Street J J, Sabey B R and Lindsay W L 1978 The influence of pH, phosphorus, cadmium, sewage sludge and incubation time on the stability and plant uptake of cadmium. J. Environ. Qual. 7, 286–290.

    Google Scholar 

  • Szmigielska A M, Van Rees K C J, Cieśliński G, and Huang P M 1996 Low molecular weight dicarboxylic acids in rhizosphere soil of durum wheat. J. Agric. Food Chem. 44, 1036–1040.

    Google Scholar 

  • Szmigielska A M, Van Rees K C J, Cieśliński G, and Huang P M 1997 Comparison of liquid and gas chromatography for analysis of low molecular weight organic acids in rhizosphere soil. Commun. Soil Sci. Plant Anal. 28, 99–111.

    Google Scholar 

  • Uren N C and Raisenauer H M 1988 The role of root exudates in nutrient acquisition. Adv. Pl. Nutr. 3, 79–114.

    Google Scholar 

  • Vancura V 1964 Root exudation of plants I. Analysis of root exudates of barley and wheat in their initial phases of growth. Plant Soil 21, 231–248.

    Google Scholar 

  • Vogeli-Lange R and Wagner G J 1990 Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiol. 92, 1086–1093.

    Google Scholar 

  • Zang F, Romheld V and Marschner H 1991 Release of zinc mobilizing root exudates in different plant species as affected by zinc nutritional status. J. Plant. Nutr. 14(7) 675–686.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cieśliński, G., Van Rees, K., Szmigielska, A. et al. Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant and Soil 203, 109–117 (1998). https://doi.org/10.1023/A:1004325817420

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004325817420

Navigation