The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens
Introduction
Soils can become contaminated with Zn from metalliferous mining wastes, smelters, refractories, industry, galvanized metalwork, sewage sludge and excess fertilization (Vangronsveld and Cunningham, 1998). Zinc-contaminated soils are a concern when plants are unable to be successfully grown either for agriculture, mine-site stabilization or urban purposes as a result of Zn phytotoxicity. Remediation of contaminated soils can be achieved by either removal of the contaminated soil, dilution with cleaner soil, or chelate/acid-washing of the soil to remove the Zn. However, these methods destroy the soil structure, often introduce new contaminants, and can be expensive (Vangronsveld and Cunningham, 1998). Alternatively, contaminated soils can be remediated using phytoextraction. Zinc phytoextraction is based upon enhanced Zn uptake by Zn-tolerant plants, and then harvest of the Zn-containing shoot biomass. This method is applicable to sites where other remediation options are uneconomical or unavailable and the timeframe for phytoremediation is acceptable. Currently, phytoremediation is being researched to increase phytoextraction and hence to decrease the time and financial cost for site remediation.
Thlaspi caerulescens is a Zn hyperaccumulator (Baker and Brooks, 1989) which typically produces a small biomass in the range 140–360 mg plant−1 (Knight et al., 1997), and shows much variability in growth rate and biomass potential in its natural populations (Bennett et al., 1998). Treatments which increase shoot biomass, without reducing Zn concentration in shoots, have the potential to enhance Zn phytoextraction.
Plants can only extract Zn from soil in the soluble form (Marschner, 1995). Therefore, Zn uptake depends upon Zn solubility, which can be increased by three common methods: acidification, complexation with chelates and Zn desorption or dissolution when the soluble Zn fraction is depleted. Zinc becomes 100 times more soluble for each unit of pH decreased from around pH 8 due to dissolution and desorption (Basta and Tabatabai, 1992, Stumm and Morgan, 1996, Adriano, 2001). Thus rhizosphere acidification should increase the soluble Zn concentration directly in the rhizosphere where it can improve phytoextraction and reduce remediation time (Brown et al., 1994). Rhizosphere acidification is preferable to acidification of the bulk soil because Zn and other co-occurring heavy metals are less likely to leach further into the environment. Furthermore, T. caerulescens is capable of depleting soluble zinc fractions (1 M NH4NO3), resulting in Zn mobilization from less available fractions in a passive equilibration of solid and solution phases (Whiting et al., 2001).
Nitrogen fertilization has been shown to increase shoot biomass and enhance Zn extraction (Ebbs et al., 1997, Bennett et al., 1998, Schwartz et al., 2003). A greater shoot biomass provides more leaf area for storage of sequestered Zn thus enhancing total Zn content per plant. The chemical form of N taken up by a plant can distinctly influence the rhizosphere pH (Nye, 1981, Gijsman, 1990, Tang and Rengel, 2003). Nitrogen can be absorbed by plant roots as , or as neutral urea (NH2)2CO. Urea can also be hydrolyzed by microbially produced urease into . When plants take up , there are more cations than anions taken into the root cells. Consequently, H+ is exuded to regulate cytosolic pH and charge balance, and the rhizosphere pH decreases. In contrast, uptake of can cause H+ influx (or OH− efflux) with a rhizosphere pH increase, while neutral urea causes little pH change (Nye, 1981, Haynes, 1990, Mengel and Kirkby, 2001, Hinsinger et al., 2003). Fertilization with (NH4)2SO4 and subsequent rhizosphere acidification enhanced Zn accumulation in non-accumulators such as willow cultivars (Salix viminalis L.), field bean (Phaseolus vulgaris L. cv. Saxa), radish (Raphanus sativus L.) and barley (Hordeum vulgare L., cv. Dorirumugi) (Sarkar and Jones, 1982a, Sarkar and Jones, 1982b, Youssef and Chino, 1989, Thomson et al., 1993, Lorenz et al., 1994, Kashem and Singh, 2002, Schmidt, 2003). In contrast, Schwartz et al. (2003) observed that (NH4)2SO4 fertilization reduced Zn accumulation and shoot dry weight in the hyperaccumulator T. caerulescens compared to NaNO3. However, they did not compare these findings with the rhizosphere pH.
Ethylenediaminedisuccinic acid (EDDS) is a naturally occurring aminopolycarboxylic acid produced by actinomycetes, and is often used as a biodegradable chelator for transition metal phytoextraction (Nishikiori et al., 1994, Bucheli-Witschel and Egli, 2001). The EDDS forms stable hexadentate complexes with transition metals (Vandevivere et al., 2001), and increases the concentration of total soluble Zn (Zn2+ and Zn–EDDS) in the soil solution. It has been shown to enhance Zn phytoextraction (Meers et al., 2005, Luo et al., 2006, Tandy et al., 2006), and was included in this study to compare its phytoextraction efficiency against the proposed fertilization method. EDDS is preferred over the historically favored EDTA for chelate-assisted phytoextraction since EDTA persists in the soil where it contributes to further contamination by nutrient and heavy metal leaching. The effectiveness of EDDS for Zn phytoextraction is dependent on four main factors: the presence of other competing metals and ions which may react with EDDS in preference to Zn, the activities of these metals in solution, the concentration of EDDS, and the solution pH. In contrast to the benefits of EDDS-assisted phytoextraction, EDDS is currently expensive to apply at the required rates, and metal-EDDS complexes have been found to degrade much more slowly than the tri-sodium complex form which is applied initially (Vandevivere et al., 2001).
The aim of this study was to compare the effect of three different N fertilizers and a chelator on rhizosphere pH, and Zn uptake by T. caerulescens. A nitrification inhibitor was used to maintain the form of N available for uptake. We also aimed to understand the mechanisms associated with enhanced Zn extraction. We hypothesized that T. caerulescens would respond to fertilization by an acidification of the rhizosphere, and to by rhizosphere alkalization, while acidification would favor Zn phytoextraction.
Section snippets
Soil collection and characterization
A Zn-contaminated soil (377 ± 20 mg Zn kg−1) was collected from the A horizon beneath a galvanized electricity pylon at Narre Warren, Victoria. The soil was sandy loam. The soil was air-dried, crushed to pass through a 2 mm sieve and mixed with washed river sand to obtain a homogenous soil with approximately 250 mg Zn kg−1. Selected properties of the final soil mixture are listed in Table 1.
Experimental design
A randomized pot experiment was conducted in a temperature-controlled glasshouse (20 ± 5 °C) with natural light.
Plant growth
All plants appeared healthy during growth, with an apparent difference in shoot biomass and color between the treatments, and very little difference within treatments and within each pot. The control and EDDS-treated plants, which received no N fertilizer, appeared paler than the other treatments. After the EDDS treatment, the leaves wilted and began to senesce. The DCD-treated plants showed some chlorosis of leaf-tips. The average shoot dry weights ranged from 0.17 to 0.38 g plant−1, and were
Discussion
This study illustrated that rhizosphere acidification did not enhance Zn extraction by T. caerulescens grown in a mildly acid soil. A contradictory result to our hypothesis was that a higher rhizosphere pH enhanced Zn extraction. This occurred with application of Ca(NO3)2 and was associated with an increased Zn content.
Enhanced shoot biomass following N fertilization improved Zn extraction by this typically low biomass species. An important result was the >100% increase in dry weight of
References (50)
- et al.
Environmental fate and microbial degradation of aminopolycarboxylic acids
FEMS Microbiol. Rev.
(2001) - et al.
Comparison of EDTA and EDDS as potential soil amendments for enhanced phytoextraction of heavy metals
Chemosphere
(2005) - et al.
The influence of EDDS on the uptake of heavy metals in hydroponically grown sunflowers
Chemosphere
(2006) - et al.
Localization of zinc and cadmium in Thlaspi caerulescens (Brassicaceae), a metallophyte that can hyperaccumulate both metals
J. Plant Physiol.
(1992) Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability and Risks of Metals
(2001)- et al.
Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry
Biorecovery
(1989) - et al.
Effect of cropping systems on adsorption of metals by soils: II. Effect of pH
Soil Sci. Soc. Am. J.
(1992) - et al.
Fertilisation of hyperaccumulators to enhance their potential for phytoremediation and phytomining
- et al.
Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures
Plant Soil.
(1991) - et al.
Phytoremediation potential of Thlaspi caerulescens and Bladder Campion for zinc- and cadmium-contaminated soil
J. Environ. Qual.
(1994)
Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens and metal tolerant Silene vulgaris grown on sludge-amended soils
Environ. Sci. Technol.
Effects of temperature and application rate of a nitrification inhibitor, dicyandiamide (DCD), on nitrification rate and microbial biomass in a grazed pasture soil
Aust. J. Soil Res.
Phytoextraction of cadmium and zinc from a contaminated soil
J. Environ. Qual.
Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens
Plant Cell Environ.
Rhizosphere pH along different root zones of Douglas fir (Pseudotsuga menziesii), as affected by source of nitrogen
Plant Soil.
Ethylenediaminedissuccinate as a new chelate for environmentally safe enhanced lead extraction
J. Environ. Qual.
Active ion uptake and maintenance of cation–anion balance. A critical examination of their role in regulating rhizosphere pH
Plant Soil.
Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review
Plant Soil.
Phytoremediation of lead-contaminated soils: Role of synthetic chelates in lead phytoextraction
Environ. Sci. Technol.
The effect of fertilizer additions on the solubility and plant-availability of Cd, Ni and Zn in soil
Nutr. Cycl. Agroecosys.
Zinc and cadmium uptake by the hyperaccumulator Thlaspi caerulescens in contaminated soils and its effects on the concentration and chemical speciation of metals in soil solution
Plant Soil.
Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi
Plant Physiol.
Applications of fertilizer cations affect cadmium and zinc concentrations in soil solutions and uptake by plants
Eur. J. Soil Sci.
A novel strategy using biodegradable EDDS for the chemically enhanced phytoextraction of soils contaminated with heavy metals
Plant Soil.
Mineral Nutrition of Higher Plants
Cited by (56)
Biofertilizer derived from dairy manure increases raspberry fruit weight and leaf magnesium concentration
2022, Scientia HorticulturaeThe combined use of arbuscular mycorrhizal fungi, biochar and nitrogen fertilizer is most beneficial to cultivate Cichorium intybus L. in Cd-contaminated soil
2021, Ecotoxicology and Environmental SafetyExogenous nitrogen enhances poplar resistance to leaf herbivory and pathogen infection after exposure to soil cadmium stress
2021, Ecotoxicology and Environmental SafetyCitation Excerpt :The ammonium ion further lead to desorption of heavy metals from exchange sites or soil colloids via ion exchange, which could increase metal bioavailability and in turn improving metal extraction and accumulation in plant organs (Lorenz et al., 1994; Lasat, 2007). However, some other studies found N fertilization resulted in a lower metal accumulation in plants due to metal dilution in leaves caused by increased plant biomass production or competition with the N fertilizers in the rhizosphere (Monsant et al., 2008; Xie et al., 2009; Jacobs et al., 2018). Jacobs et al. (2019) argued that N input increase trace metal uptake only at higher doses (e.g. 80–150 mg kg−1), while at lower doses of N (e.g. 30 mg kg−1) it has no positive effect on metal uptake.
Nitrogen combined with biochar changed the feedback mechanism between soil nitrification and Cd availability in an acidic soil
2020, Journal of Hazardous MaterialsRegulatory mechanisms of nitrogen (N) on cadmium (Cd) uptake and accumulation in plants: A review
2020, Science of the Total Environment