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Soil, land care and environmental research
RESEARCH ARTICLE

Cadmium-induced changes in soil biochemical characteristics of oat (Avena sativa L.) rhizosphere during early growth stages

Stefania Astolfi A D , Sabrina Zuchi A , Fabrizio De Cesare B , Luigi Badalucco C and Stefano Grego A
+ Author Affiliations
- Author Affiliations

A DAFNE, Università degli Studi della Tuscia, Via S. C. de Lellis, I-01100 Viterbo, Italy.

B DIBAF, Università degli Studi della Tuscia, Via S. C. de Lellis, I-01100 Viterbo, Italy.

C Dipartimento dei Sistemi Agro-Ambientali, Università degli Studi di Palermo, Viale delle Scienze 13, I-90128 Palermo, Italy.

D Corresponding author. Email: sastolfi@unitus.it

Soil Research 49(7) 642-651 https://doi.org/10.1071/SR11158
Submitted: 30 June 2010  Accepted: 18 October 2011   Published: 17 November 2011

Abstract

A microcosm was assembled to physically separate soil from roots and was used to study both the impact of living roots on the soil–plant system during early stages of growth and plant responses to abiotic stress. Oat (Avena sativa L.) seedlings were grown in the microcosm unit for 44 days. Twenty-three days after planting, 0.154 mg CdSO4/g dry soil was added. Plants grown in Cd-treated microcosms showed considerable inhibition of shoot growth rates, and leaf chlorophyll content. Soil microbial biomass C and respiration increased with plant age, and most of the measured biochemical indicators decreased with increasing distance from the soil–root interface, thus demonstrating the rhizosphere effect, likely due to the quick assimilation of rhizodeposits by rhizosphere microflora. On the other hand, short-term Cd contamination sometimes had an inhibitory effect on soil respiration, qCO2, ATP content, and phosphatase activity, while stimulating microbial biomass, mainly at the rhizosphere level. The decrease in rhizosphere microbial activity observed after Cd application to soil may be due to a synergic effect of the metal directly on microbial cells and indirectly on plants, which reduced shoot growth rate and chlorophyll content, resulting in decreased availability of root exudates.

Additional keywords: heavy metals, microbial activity, microbial biomass, Cd, rhizosphere, oat.


References

Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology & Biochemistry 25, 393–395.
The metabolic quotient for CO2 (qCO2) as a specific parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils.Crossref | GoogleScholarGoogle Scholar |

Asmar F, Eiland F, Nielsen NE (1992) Interrelationship between extracellular enzyme activity, ATP content, total counts of bacteria and CO2 evolution. Biology and Fertility of Soils 14, 288–292.
Interrelationship between extracellular enzyme activity, ATP content, total counts of bacteria and CO2 evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVOrt7k%3D&md5=2fd1fb10961549eae74ea539e225c503CAS |

Astolfi S, Zuchi S, Passera C (2004) Effects of Cd on the metabolic activity of Avena sativa plants grown in soil or hydroponic culture. Biologia Plantarum 48, 413–418.
Effects of Cd on the metabolic activity of Avena sativa plants grown in soil or hydroponic culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVeltrk%3D&md5=a1c7bbcfc8cf893bda75ce36caa86386CAS |

Bååth E, Arnebrandt K, Nordgren A (1991) Microbial biomass and ATP in smelter-polluted forest humus. Bulletin of Environmental Contamination and Toxicology 47, 278–282.
Microbial biomass and ATP in smelter-polluted forest humus.Crossref | GoogleScholarGoogle Scholar |

Badalucco L, Grego S, Dell’Orco S, Nannipieri P (1992) Effect of liming on some chemical, biochemical and microbiological properties of acid soils under spruce (Picea abies L.). Biology and Fertility of Soils 14, 76–83.
Effect of liming on some chemical, biochemical and microbiological properties of acid soils under spruce (Picea abies L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvVOnsQ%3D%3D&md5=ec7aa7df66e02a503497f610166de971CAS |

Badalucco L, Kuikman PJ, Nannipieri P (1996) Protease and deaminase activities in wheat rhizosphere and their relation to bacterial and protozoan populations. Biology and Fertility of Soils 23, 99–104.
Protease and deaminase activities in wheat rhizosphere and their relation to bacterial and protozoan populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmvVWisb0%3D&md5=b4914c2d562008814678a8ca74aaa3f2CAS |

Badalucco L, Nannipieri P (2007) Nutrient transformations in the rhizosphere. In ‘The rhizosphere: biochemistry and organic substances at the soil–plant interface’. 2nd edn (Eds R Pinton, Z Varanini, P Nannipieri) pp. 111–133. (Taylor & Francis: Boca Raton, FL)

Bremner JM, Tabatabai MA (1973) Effects of some inorganic constituents on TTC assay of dehydrogenase activity in soils. Soil Biology & Biochemistry 5, 385–386.
Effects of some inorganic constituents on TTC assay of dehydrogenase activity in soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGit7c%3D&md5=085129e21e0d27874d9405dc7f3af3f2CAS |

Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil 329, 1–25.
Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFGks7o%3D&md5=5b7d0cc00ade188a66d07e7fb949b285CAS |

Chander K, Brookes PC (1991) Microbial biomass dynamics during the decomposition of glucose and maize in metal-contaminated and non-contaminated soils. Soil Biology & Biochemistry 23, 917–925.
Microbial biomass dynamics during the decomposition of glucose and maize in metal-contaminated and non-contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVajtw%3D%3D&md5=63746cbf55130233da638a2b34537ee2CAS |

Chander K, Brookes PC, Harding SA (1995) Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam. Soil Biology & Biochemistry 27, 1409–1421.
Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1yiu7k%3D&md5=858cf2e80b4ded6303710b8631e3b0afCAS |

Dar GH (1996) Effects of cadmium and sewage-sludge on soil microbial biomass and enzyme activities. Bioresource Technology 56, 141–145.
Effects of cadmium and sewage-sludge on soil microbial biomass and enzyme activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVyit70%3D&md5=7f4be4095e71f202e183003fc974b94dCAS |

De Cesare F, Garzillo AMV, Buonocore V, Badalucco L (2000) Use of sonication for estimating acid phosphatase activity in soil. Soil Biology & Biochemistry 32, 825–832.
Use of sonication for estimating acid phosphatase activity in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFWjtrs%3D&md5=30a4457cfda46b5e68e714181dc2a1b7CAS |

Dick RP (1997) Soil enzyme activities as integrative indicators of soil health. In ‘Biological indicators of soil health’. (Eds CE Pankhurst, BM Doube, VVSR Gupta) pp. 121–156. (CAB International: Wallingford, UK)

Fließbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge. Soil Biology & Biochemistry 26, 1201–1205.
Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge.Crossref | GoogleScholarGoogle Scholar |

Gahoonia TS, Claassen N, Jungk A (1992) Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate. Plant and Soil 140, 241–248.
Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate.Crossref | GoogleScholarGoogle Scholar |

Garcia C, Hernandez T, Costa F (1997) Potential use of dehydrogenase activity as an index of microbial activity in degraded soils. Communications in Soil Science and Plant Analysis 28, 123–134.
Potential use of dehydrogenase activity as an index of microbial activity in degraded soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Gnsbc%3D&md5=378a746dafbd55f63d34df478fd803c2CAS |

Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218, 159–171.
The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVGrtLc%3D&md5=ce9bc06899566afeae292842d60c3fe6CAS |

Gil-Sotres F, Trasar-Cepeda C, Leiròs MC, Seoane S (2005) Different approaches to evaluating soil quality using biochemical properties. Soil Biology & Biochemistry 37, 877–887.
Different approaches to evaluating soil quality using biochemical properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVSltLk%3D&md5=148e733190053852acc261a053fa5b08CAS |

Gregory PJ, Hinsinger P (1999) New approaches to studying chemical and physical changes in the rhizosphere: an overview. Plant and Soil 211, 1–9.
New approaches to studying chemical and physical changes in the rhizosphere: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Krtro%3D&md5=ec8ddcf092ebbdc94ccacdb9878d1f9bCAS |

Haanstra L, Doelman P (1991) An ecological dose-response model approach to short-term and long-term effects of heavy metals on arylsulphatase activity in soil. Biology and Fertility of Soils 11, 18–23.
An ecological dose-response model approach to short-term and long-term effects of heavy metals on arylsulphatase activity in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlt12nsLs%3D&md5=69a4b8c6586ee784da93a8657b99cc30CAS |

Hattori H (1988) Microbial activities in soil amended with sewage sludge. Soil Science and Plant Nutrition 34, 221–232.

Hinojosa MB, Carreira JA, García-Ruíz R, Dick R (2004) Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biology & Biochemistry 36, 1559–1568.
Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslKhtrg%3D&md5=f693ff6fda6d267b4baaff7881960d5eCAS |

Hinsinger P (1998) How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. Advances in Agronomy 64, 225–265.
How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsVOq&md5=51ce71e091f2fac22455a5c9cf4b378dCAS |

Hinsinger P, Gilkes RJ (1996) Mobilization of phosphate from phosphate rock and alumina-sorbed phosphate by the roots of ryegrass and clover as related to rhizosphere pH. European Journal of Soil Science 47, 533–544.
Mobilization of phosphate from phosphate rock and alumina-sorbed phosphate by the roots of ryegrass and clover as related to rhizosphere pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtFGjsbc%3D&md5=34d57b01657ea87ec4c6bd36e2a77ad7CAS |

Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist 168, 293–303.
Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Smu7bJ&md5=e372818dd49e2005e2a8bce992fa5106CAS |

Hoagland DR, Arnon DL (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station Circular No. 347.

Jacobson KB, Turner JE (1980) The interaction of cadmium and certain other metal ions with proteins and nucleic acids. Toxicology 16, 1–37.
The interaction of cadmium and certain other metal ions with proteins and nucleic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXltVyisrw%3D&md5=e087fe39c50de3ea2231997e79ab9d63CAS |

Jaillard B, Plassard C, Hinsinger P (2002) Measurements of H+ fluxes and concentrations in the rhizosphere. In ‘Handbook of soil acidity’. (Ed. Z Rengel) pp. 231–266. (Marcel Dekker: New York)

Jenkinson DS (1988) Determination of microbial biomass carbon and nitrogen in soil. In ‘Advance in nitrogen cycling in agricultural ecosystems’. (Ed. JR Wilson) pp. 368–386. (Commonwealth Agricultural Bureau International: Wallingford, UK)

Khan M, Scullion J (2000) Effect of soil on microbial responses to metal contamination. Environmental Pollution 110, 115–125.
Effect of soil on microbial responses to metal contamination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFyiur0%3D&md5=3384de57aa7924914387c422d968c137CAS |

Krupa Z, Baszynski T (1995) Some aspect of heavy metals toxicity towards photosynthetic apparatus direct and indirect effects on light and dark reactions. Acta Physiologiae Plantarum 17, 177–190.

Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant and Soil 200, 241–250.
Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFWksbk%3D&md5=f655ef7e809227d1e578f084ae6a390cCAS |

Lee I-S, Kim OK, Chang Y-Y, Bae B, Kim HH, Baek KH (2002) Heavy metal concentrations and enzyme activities in soil from a contaminated Korean shooting range. Journal of Bioscience and Bioengineering 94, 406–411.

Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Kandeler E (2006) Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biology & Biochemistry 38, 1430–1437.
Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVOnsb4%3D&md5=181ae27f2eda4fcaf90632221d807733CAS |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ 2nd edn (Academic Press Ltd: London)

McBride MB (1994) ‘Environmental chemistry of soils.’ (Oxford University Press: New York)

Mühlbachová G, Simon T (2003) Effects of zeolite amendment on microbial biomass and respiratory activity in heavy metal contaminated soils. Plant, Soil and Environment 49, 536–541.

Nannipieri P, Badalucco L, Landi L, Pietramellara G (1997) Measurement in assessing the risk of chemicals to the soil ecosystem. In ‘Ecotoxicology: responses, biomarkers, and risk assessment. An OECD Workshop’. (Ed. JT Zelikoff) pp. 1–28. (SOS Publications: Fair Haven, NJ)

Nannipieri P, Grego S, Ceccanti B (1990) Ecological significance of the biological activity in soil. In ‘Soil biochemistry’. (Eds JM Bollag, G Stotzky) pp. 293–355. (Marcel Dekker: New York)

Obbard P (2001) Ecotoxicological assessment of heavy metals in sewage sludge amended soils. Applied Geochemistry 16, 1405–1411.
Ecotoxicological assessment of heavy metals in sewage sludge amended soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslamtL4%3D&md5=9b38d800867e3b06700cf8ff227cbab8CAS |

Odum EP (1985) Trends expressed in stressed ecosystems. Bioscience 35, 419–422.
Trends expressed in stressed ecosystems.Crossref | GoogleScholarGoogle Scholar |

Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil microbial characteristics. Journal of Bioscience and Bioengineering 102, 157–161.
Effects of long-term heavy metal contamination on soil microbial characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ahsb3F&md5=76827d2ad9ab34fdf39cf07309105a2dCAS |

Pinton R, Varanini Z, Nannipieri P (2007) ‘The rhizosphere—biochemistry and organic substances at the soil–plant interface.’ 2nd edn (Taylor & Francis: Boca Raton, FL)

Prasad MNV (1995) Cd toxicity and tolerance in vascular plants. Environmental and Experimental Botany 35, 525–545.
Cd toxicity and tolerance in vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1agsbc%3D&md5=c612b107d1c2eedcf9b2c5fff53caa9eCAS |

Prassad DDK, Prassad ARK (1987) Altered δ-aminolaevulinic acid metabolism by lead and mercury in germinating seedlings of Bajra (Pennisetum typhoideum). Journal of Plant Physiology 127, 241–249.

Renella G, Ortigoza ALR, Landi L, Nannipieri P (2003) Additive effects of copper and zinc on Cd toxicity on phosphatase activities and ATP content of soil as estimated by ecological dose (ED50). Soil Biology & Biochemistry 35, 1203–1210.
Additive effects of copper and zinc on Cd toxicity on phosphatase activities and ATP content of soil as estimated by ecological dose (ED50).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVCmtb4%3D&md5=36be6ba32bfda61949622861d2f46822CAS |

Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytologist 127, 635–674.
The responses of plants to non-uniform supplies of nutrients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsFCmu7Y%3D&md5=490941fb9cf685be5301172bc6bae394CAS |

Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environmental and Experimental Botany 41, 105–130.
Response to cadmium in higher plants.Crossref | GoogleScholarGoogle Scholar |

Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology & Biochemistry 1, 301–307.
Use of p-nitrophenyl phosphate for assay of soil phosphatase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhtFShu7Y%3D&md5=4971b7cdf1d483605c8357934320701fCAS |

Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant and Soil 155–156, 95–98.
Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots.Crossref | GoogleScholarGoogle Scholar |

Tomasi N, Weisskopf L, Renella G, Landi G, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biology & Biochemistry 40, 1971–1974.
Flavonoids of white lupin roots participate in phosphorus mobilization from soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1ektLw%3D&md5=b2dae9f96ea3b2e04900f756d99ade22CAS |

Tyler G, Olsson T (2001) Concentrations of 60 elements in the soil solution as related to the soil acidity. European Journal of Soil Science 52, 151–165.
Concentrations of 60 elements in the soil solution as related to the soil acidity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXislCrurY%3D&md5=d1ec5013e67ab2e20588f69370ca87f3CAS |

Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring microbial biomass carbon. Soil Biology & Biochemistry 19, 703–707.
An extraction method for measuring microbial biomass carbon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjs1KqsA%3D%3D&md5=5f9f5eeab2e6bc230e9ae7925eadb8ccCAS |

Wagner GJ (1993) Accumulation of Cd in crop plants and its consequences to human health. In ‘Advances in agronomy’. (Ed. DL Sparks) pp. 173–212. (Academic Press Inc.: California)

Wardle DA, Ghani A (1995) A critique of the microbial quotient (qCO2) as a bio-indicator of disturbance and ecosystem development. Soil Biology & Biochemistry 27, 1601–1610.
A critique of the microbial quotient (qCO2) as a bio-indicator of disturbance and ecosystem development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSntrfM&md5=1f91b4fde6a42c6601893b037d76dfb6CAS |

Webster JJ, Hampton GJ, Leach FR (1984) ATP in soil: a new extractant and extraction procedure. Soil Biology & Biochemistry 16, 335–342.
ATP in soil: a new extractant and extraction procedure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlvFSgsbY%3D&md5=800696efd58b25a97c0b36e2f245e7d9CAS |