Journal of Plant Nutrition and Soil Science

Regular Article

Full Access

Response of white mustard (Sinapis alba) and the soil microbial biomass to P and Zn addition in a greenhouse pot experiment

Khalid Saifullah Khan

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, Germany

Permanent address: Department of Soil Science, PMAS-Arid Agriculture University, Murree Road, 46300 Rawalpindi, Pakistan

Search for more papers by this author

Rainer Georg Joergensen,

Corresponding Author

Rainer Georg Joergensen

[email protected]

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, Germany

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, GermanySearch for more papers by this author

Khalid Saifullah Khan,

Khalid Saifullah Khan

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, Germany

Permanent address: Department of Soil Science, PMAS-Arid Agriculture University, Murree Road, 46300 Rawalpindi, Pakistan

Search for more papers by this author

Rainer Georg Joergensen,

Corresponding Author

Rainer Georg Joergensen

[email protected]

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, Germany

Department of Soil Biology and Plant Nutrition, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, GermanySearch for more papers by this author

First published: 01 October 2015

https://doi.org/10.1002/jpln.201500129

Citations: 8

Share a link

Email
Wechat
Bluesky

Abstract

A 45-d pot experiment was carried out to investigate the response of white mustard and the soil microbial biomass after Zn and P addition to a P deficient silt loam. The underlying hypothesis was that P application reduces the Zn availability to crops and microbial biomass. White mustard was supplied with different levels of P (0, 50, and 100 µg g⁻¹ soil) and Zn (0, 10, and 20 µg g⁻¹ soil). Amendments of P generally reduced extractable Zn, shoot Zn and soil microbial biomass Zn. Amendments of P generally decreased the microbial biomass C/P ratio. At 20 µg Zn g⁻¹ soil, a negative effect on the microbial biomass C/P ratio was observed, suggesting that high contents of extractable Zn have a negative impact on the microbial P uptake. However, the minimum Zn requirements of soil microorganisms and the consequences of microbial Zn deficiency for soil microbiological processes are completely unknown.

1 Introduction

Crop nutrition relies very much on soil microorganisms as they decompose organic matter (OM), release nutrients to plants, and store macronutrients such as P (Brookes et al., 1982) but also micronutrients such as Zn in their biomass (Wallander et al., 2003; Khan et al., 2009), protecting them against fixation by inorganic soil components (Khan et al., 2012). Phosphorus deficiency not only restricts crop growth but has also been found to have a negative impact on the microbial energy metabolism leading to low ATP to microbial biomass C ratios (Salamanca et al., 2006). Zinc deficiency is also very common in many parts of the world, affecting, e.g., nearly 50% of the cereal production areas in the world (Cakmak, 2008). Zinc is an essential micronutrient for numerous physiological processes as it serves as a cofactor in many enzymes and in the maintenance of protein structure in plants, animals, fungi, and bacteria (Blencowe and Morby, 2003).

In many soils, Zn deficiency is combined with P deficiency (Cakmak, 2008; Khan and Joergensen, 2010) causing problems for crop fertilization as there are negative interactions between these two nutrients (Loneragan et al., 1982; Barrow, 1987). High contents of extractable P reduce Zn availability to plants (Cakmak and Marschner, 1986; Zhang et al., 2012), whereas high contents of extractable Zn may reduce P availability to soil microorganisms as indicated by high microbial biomass C/P ratios in Zn contaminated soils (Khan et al., 2007).

Despite the importance for physiological processes, excessive contents of Zn have significant toxicity and act as a potent disrupter of biological systems (Blencowe and Morby, 2003), e.g., in soils contaminated by sewage sludge, mining dumps, and industrial exhaust gases (Chander et al., 2001a, b). A lot of research has been carried out on Zn toxicity to soil microorganisms (Chander and Brookes, 1991; He et al., 2005), but not much is known about microbial micronutrient deficiency, although soil bacteria and soil fungi certainly also have a demand for Zn (White and Gadd, 1987; Wallander et al., 2003; Khan and Joergensen, 2010).

A pot experiment was designed to investigate the response of white mustard (Sinapis alba L.) and the soil microbial biomass after Zn and P addition to a silt loam with low total P content. White mustard has a strong capacity to take up large amounts of P and Zn, increasing any existing limitations of soil microorganisms (Föhse et al., 1988; Khan et al., 2012). The underlying hypothesis was that P amendment reduces the Zn availability to both crops and microbial biomass. However, this reduced Zn availability might be counteracted by moderate application rates of Zn.

2 Material and methods

2.1 Soil

The soil was taken in September 2012 at 0–15 cm depth from the site “Saurasen” (Quintern et al., 2006) in N Hessia, Germany, sieved (< 2 mm), homogenized, and stored in polyethylene buckets at room temperature for about 1 week before the experiment started. The soil (6% sand, 77% silt, 17% clay) has been developed from eroded loess overlying clayey New Red Sandstone and was classified as Stagnic Luvisol according to the WRB-FAO classification system (FAO, 2014). The soil had a pH of 6.5 in water and contained 9.8 mg soil organic C (SOC), 1.0 mg total N, 370 µg total P, 0.66 mg oxalate extractable Al, 0.77 dithionite extractable Al, 2.2 mg oxalate extractable Fe, 7.5 mg dithionite extractable Fe, 9.1 µg 0.5 M NaHCO₃ extractable P (Khan and Joergensen, 2012), and 0.43 µg NH₄NO₃ extractable Zn g⁻¹ soil.

2.2 Pot experiment

The experiment consisted of two factors (P and Zn addition) distributed over 9 experimental treatments, each with three replicates (in µg g⁻¹ soil): (1) +P-0 + Zn-0, (2) +P-0 + Zn-10, (3) +P-0 + Zn-20, (4) +P-50 + Zn-0, (5) +P-50 + Zn-10, (6) + P-50 + Zn-20, (7) +P-100 + Zn-0, (8) +P-100 + Zn-10, and (9) + P-100 + Zn-20. To reach the respective contents in soil, 50 µg P and 100 µg P g⁻¹ soil were added as KH₂PO₄ solution, whereas 10 µg Zn and 20 µg Zn g⁻¹ soil were adjusted with ZnSO₄ · 7 H₂O solution. Additionally, 200 µg N as NH₄NO₃ and 100 µg K as K₂SO₄ g⁻¹ soil were applied to each pot, containing 2.0 kg (on an oven-dry basis) of soil. Three seeds of white mustard (Sinapis alba L. variety SITO) were sown at a depth of 0.5 cm. After emergence, plants were screened out so that each pot maintained two healthy plants. The pots were arranged in a completely randomized design and placed in a temperature-controlled greenhouse chamber with a 16–8 h light-dark cycle and a mean temperature of 25°C (day) and 12°C (night). The moisture was kept at 50% of the soil water holding capacity by weighing the pots twice a week and adding the water lost regularly. The experiment started on September 24, 2012, and was carried out until November 8, 2012. After the final harvest at day 45, the soil was sieved (< 2 mm) after removing the roots. Soil adhering to roots on top of the sieve was carefully removed from the roots and passed through the sieve. Separated roots were removed, rinsed with distilled water, dried and weighed.

2.3 Analytical procedures

Microbial biomass C was estimated by the fumigation-extraction method using 0.5 M K₂SO₄ as extractant (Vance et al., 1987). Microbial biomass C was calculated as E_C / k_EC, where E_C = (organic C extracted from fumigated soils) – (organic C extracted from non-fumigated soils) and k_EC = 0.45 (Wu et al., 1990). Soil microbial biomass P was also measured by the fumigation-extraction method using 0.5 M NaHCO₃ (pH 8.5) as extractant (Brookes et al., 1982) as described by Joergensen et al. (1995). Microbial biomass P was calculated as E_P / k_EP / recovery, where E_P = (PO₄-P extracted from fumigated soil) – (PO₄-P extracted from non-fumigated soil) and k_EP = 0.40 (Brookes et al., 1982). Microbial biomass Zn was determined by extracting 10 g moist soil (on an oven-dry basis) with 50 mL 1 M NH₄NO₃ as described by Khan et al. (2009). Zinc in the extracts was determined by ICP-AES (Spectro Analytical Instruments, Kleve, Germany). Then, microbial biomass Zn was calculated as E_Zn = (Zn extracted from fumigated soil) – (Zn extracted from non-fumigated soil) without applying a conversion values.

Contents of 0.5 M NaHCO₃-extractable PO₄-P and 1 M NH₄NO₃ extractable Zn obtained from the non-fumigated soil by the fumigation-extraction method were taken as indices for the mobile (= plant available) fraction of total P (Joergensen et al., 1995) and total Zn (Chander et al., 2008; Krpata et al., 2009), respectively. In soil and plant material, total P and total Zn concentrations were determined by HNO₃-pressure digestion as described by Chander et al. (2008) and measured by ICP-AES.

2.4 Statistical Analysis

The results presented in the tables are arithmetic means and expressed on an oven-dry basis (about 24 h at 105°C). Normal distribution of data and residues was tested by the Shapiro–Wilk test and equal variance by the Brown–Forsythe test. The significance of treatment effects was analysed by a two-way ANOVA, followed by the Holm–Sidak method as a pair-wise multiple comparison test. All statistical calculations were carried out using SigmaPlot 13.0 (Systat Inc., San José, USA).

3 Results

In the P-50 and P-100 treatments, shoot biomass pot⁻¹ increased by 130 and 190%, respectively, in comparison with the P-0 treatment (Fig. 1a) and root biomass by 60 and 110% (Fig. 1b). Shoot P concentration additionally increased by 140 and 190% (Fig. 1c), whereas shoot Zn decreased by 52 and 66%, respectively (Fig. 1d). In the Zn-10 treatment, shoot biomass increased on average by 17% and root biomass by 30% in comparison with the Zn-0 treatment (Fig. 1a, b). The Zn-20 treatment had generally less positive effects on shoot and root biomass than the Zn-10 treatment. In the P-100/Zn-20 treatment, shoot and root biomass were even significantly lower than in the P-100/Zn-0 treatment, leading to significant P × Zn second order interactions. In the Zn-10 and Zn-20 treatments, the concentrations of shoot P decreased on average by roughly 7% in comparison with the Zn-0 treatment (Fig. 1c). The concentration of shoot Zn showed 140% and 210% increases in the Zn-10 and Zn-20 treatments, respectively, in comparison with the Zn-0 treatment (Fig. 1d).

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Parameters measured after 45-d pot experiment: (a) shoot dry weight of white mustard in the different P and Zn addition treatments, probability values: P < 0.01, Zn < 0.01, P × Zn < 0.01; (b) root dry weight, probability values: P < 0.01, Zn < 0.01, P × Zn = 0.01; (c) shoot P concentration, probability values: P < 0.01, Zn < 0.01, P × Zn = 0.07; (d) shoot Zn concentration, probability values: P < 0.01, Zn < 0.01, P × Zn < 0.01. Bars represent + 1 standard deviation; different small letters above the bar indicate a significant difference within a P level (Holm–Sidak test, P < 0.05); different capital letters above the bar indicate a significant difference within a Zn level (Holm–Sidak test, P < 0.05).

In the P-50 and P-100 treatments, NaHCO₃ extractable P increased by 20 and 43 µg P g⁻¹ soil, respectively, in comparison with the P-0 treatment (Fig. 2a). In the P-0/Zn-10 and P0-Zn-20 treatments, NH₄NO₃ extractable Zn increased by 1.7 and 4.4 µg Zn g⁻¹ soil, respectively, in comparison with the Zn-0 treatment (Fig. 2b). In the P-50 and P-100 treatments, NH₄NO₃ extractable Zn decreased by 28 and 36%, respectively. The Zn-10 treatment had variable effects on NaHCO₃ extractable P, a negative effect in the P0-treatment, no effect in the P-50, and a positive effect in the P-100 treatment (Fig. 2a). In contrast, the Zn-20 treatment generally led to an average significant 8% decrease.

In the P-50 and P-100 treatments, microbial biomass C increased by 13 and 18%, respectively, in comparison with the P-0 treatment (Fig. 3a), and microbial biomass P by 44 and 80% (Fig. 3b), whereas microbial biomass Zn decreased by 11 and 15% (Fig. 3c). The stronger increase in microbial biomass P led to significantly decreased microbial biomass C/P ratios in the P-50 and P-100 treatments (Fig. 3d). Microbial biomass P showed a significant positive linear relationship with the root biomass (r = 0.95), which was not affected by the Zn treatments (Fig. 4). In the Zn-10 treatment, microbial biomass C significantly increased on average by 11% and microbial biomass P by 14% in comparison with the Zn-0 treatment (Fig. 3a, b). In the Zn-20 treatment, microbial biomass C significantly increased on average by only 6%, whereas microbial biomass P significantly declined by 5% in comparison with the respective Zn-0 treatments. Microbial biomass Zn showed nearly 5- and 9-fold increases in the Zn-10 and Zn-20 treatments, respectively, in comparison with the Zn-0 treatment (Fig. 3c). The additional increase in microbial biomass Zn from the Zn-10 to the Zn-20 treatments was stronger in the P-50 and P-100 treatments than in the P-0 treatment, leading to a significant P × Zn second order interaction.

4 Discussion

Phosphate amendment generally reduced the Zn concentration in white mustard shoots, in soil extracts, and also in the soil microbial biomass. This negative phosphate effect has already been observed for crops (Cakmak and Marschner, 1986; Watts-Williams et al., 2014) and soil extracts (Barrow, 1987; Norvell et al., 1987; Wang and Harrell, 2005; Zhao and Selim, 2010), but not for the soil microbial biomass. However, phosphate amendment had only minor effects on Zn uptake in comparison with the P-0 treatment. On average, 3.0% of the Zn applied were taken up by the white mustard shoots in the Zn-10 and 1.9% in the Zn-20 treatments, respectively.

Phosphate amendment not only increased P concentrations, but also resulted in significantly higher plant yields and microbial biomass contents. The relative P-induced biomass increases were much stronger for plant than for microbial biomass. This suggests that the increase in microbial biomass was mainly an indirect effect of P fertilization due to the higher C input by rhizodeposits. However, plant induced increases in microbial biomass have not always been observed in pot experiments (Chen et al., 2003; Muhammad et al., 2007), whereas P application resulted in some cases in rapid increases in microbial biomass C and especially microbial biomass P (Khan and Joergensen, 2009).

Soil fungi and bacteria are able to store excess available P as polyphosphates in the cytoplasm (Gächter and Meyer, 1993; Nielsen et al., 2002), in acidocalcisomes (Docampo et al., 2005, 2010; Docampo, 2006), in fungal vacuoles (Klionsky et al., 1990), but presumably also in the teichoic acids of Gram positive bacterial cell walls (Grant, 1979; Oberson and Joner, 2005). The microbial biomass C/P ratio in the present experiment varied between 8 and 15, i.e., in the range obtained by Joergensen and Emmerling (2006) or Brookes et al. (1982) for arable soils in a temperate climate of Europe. The significant increase of the microbial biomass C/P ratio in the Zn-20 treatments suggests negative effects of Zn on the P uptake of soil microorganisms as already proposed by Khan et al. (2007), investigating the effects of heavy metal pollution on the elemental stoichiometry of the soil microbial biomass. However, in their survey the microbial biomass C/P ratio ranged from 19 to 32 in highly Zn polluted soils, i.e., similar to arable soils in the tropics and sub-tropics, very low in P availability to soil microorganisms (Ghoshal and Singh, 1995; Muhammad et al., 2008; Joergensen, 2010). This suggests that phosphate application must lower Zn toxicity to plants and soil microorganisms in highly Zn contaminated soils.

Effects of Zn on phosphate turnover were dependent on the application rate. At 10 µg Zn g⁻¹ soil, no effects on the microbial biomass C/P ratios and NaHCO₃ extractable P were measured but positive effects on plant and microbial biomass. At 20 µg Zn g⁻¹ soil, the content of extractable P decreased, suggesting counteracting Zn effects on soil P retention (Tu et al., 2002). The possibility of negative interactions between Zn and P availability has already been proposed by Khan and Joergensen (2010), investigating the microbial response to the application of 50 µg Zn g⁻¹ soil, incubating a Zn and P deficient alkaline subsoil.

Application of Zn generally increased the Zn concentration in white mustard shoots, in NH₄NO₃ extracts, and in the soil microbial biomass. On average, 3.1% of the Zn applied remained NH₄NO₃ extractable in the Zn-10 and 4.3% in the Zn-20 treatment, whereas 3.9% of the Zn applied were taken up as the CHCl₃-labile fraction by the soil microbial biomass in the Zn-10 and 3.0% in the Zn-20 treatments, respectively. Even for the Zn-0 treatment, the Zn concentration in the white mustard plants was in the middle of the range presented in literature, in which Zn concentrations between 30 and 1,200 µg g⁻¹ dry weight have been reported, partly for highly Zn contaminated soils (Płociniczak et al., 2013; Jankowski et al., 2014; Zalewska and Nogalska, 2014). This indicates that the Zn availability in the current low P soil seems to be sufficient for crop growth (Sadeghzadeh and Rengel, 2011). It also indicates that the current white mustard variety has a strong capacity for Zn uptake (Płociniczak et al., 2013), probably combined with a low Zn use efficiency (Sadeghzadeh and Rengel, 2011; Kabir et al., 2014). Although none of the white mustard plants showed any visible symptoms of Zn toxicity, the Zn-20 treatment already seems to have toxic effects not only on plant yield but also on soil microorganisms. This suggests that there is only a small range for optimum fertilization rates for highly soluble Zn salts.

NH₄NO₃-extractable and microbial biomass Zn were closely correlated, indicating that the microbial uptake is controlled by Zn availability and not by microbial Zn demand. The microbial biomass Zn contents in the current Zn-0 treatments were in the range from 13 to 105 µg Zn g⁻¹ soil as observed by Khan et al. (2009) for low metal soils. The average microbial biomass Zn content of 78 g Zn g⁻¹ soil in the Zn-0 treatments corresponds to a Zn-concentration of 170 µg g⁻¹ dry weight, assuming a C content of 45% for the soil microbial biomass. This value is nearly identical to the mean of 150 µg Zn g⁻¹ dry weight measured by Wallander et al. (2003) in fungal mycelia, using PIXE (particle induced x-ray emission) analysis of fungal mycelia growing in sand mesh-bags buried in forest soils. In fungal fruit bodies and sporophores, sampled on the soil surface, concentrations between 17 and 300 µg Zn g⁻¹ dry weight. have been repeatedly measured (Tyler, 1980; Gadd, 2007; Kalač, 2010), which are in line with the current results. A close relationship between the Zn concentrations of fungal mycelium and sporophores has been observed in Zn polluted litter layers (Krpata et al., 2009).

In soils with Zn deficiency, which is often combined with P deficiency, sole application of P fertilizers will further increase Zn deficiency to plants but also to soil microorganisms. If Zn deficiency in soil microorganisms reduces their mineralization activity, this will put additional pressure on nutrient supply to crops growing on P and Zn deficient soils. This hypothesis may be evaluated.

5 Conclusions

The application of 50 and 100 µg P g⁻¹ soil reduced the contents of extractable Zn, shoot biomass Zn, and also microbial biomass Zn, which should be considered when applying P fertilizers to P and Zn deficient soils. Application of P also decreased the microbial biomass C/P. At 20 µg Zn g⁻¹ soil a negative effect on the microbial biomass C/P ratio was observed, indicating that high contents of extractable Zn may have a negative impact on soil microbial P uptake. The minimum Zn requirements of soil microorganisms and the consequences of microbial Zn deficiency for soil microbiological processes are completely unknown.

Acknowledgements

Khalid Saifullah Khan is grateful to the Alexander von Humboldt Foundation for granting a Georg Forster fellowship. We thank Gabriele Dormann for providing skillful technical assistance.

References

Barrow, N. J. (1987): The effects of phosphate on zinc sorption by a soil. J. Soil Sci. 38, 453–459.
10.1111/j.1365-2389.1987.tb02280.x
CAS Web of Science® Google Scholar
Blencowe, D. K., Morby, A. P. (2003): Zn(II) metabolism in prokaryotes. FEMS Microbiol. Rev. 27, 291–311.
10.1016/S0168-6445(03)00041-X
CAS PubMed Web of Science® Google Scholar
Brookes, P. C., Powlson, D. S., Jenkinson, D. S. (1982): Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14, 319–329.
10.1016/0038-0717(82)90001-3
CAS Web of Science® Google Scholar
Cakmak, I. (2008): Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302, 1–17.
10.1007/s11104-007-9466-3
CAS Web of Science® Google Scholar
Cakmak, I., Marschner, H. (1986): Mechanism of phosphorus induced zinc deficiency in cotton. I. Zinc deficiency enhanced uptake rate of phosphorus. Physiol. Plant. 68, 483–490.
10.1111/j.1399-3054.1986.tb03386.x
CAS Web of Science® Google Scholar
Chander, K., Brookes, P. C. (1991): Microbial biomass dynamics during the decomposition of glucose and maize in metal-contaminated and non-contaminated soils. Soil Biol. Biochem. 23, 917–925.
10.1016/0038-0717(91)90171-F
CAS Web of Science® Google Scholar
Chander, K., Dyckmans, J., Joergensen, R. G., Meyer, B., Raubuch, M. (2001a): Different sources of heavy metals and their long-term effects on soil microbial properties. Biol. Fert. Soils 34, 241–247.
10.1007/s003740100406
CAS Web of Science® Google Scholar
Chander, K., Dyckmans, J., Hoeper, H., Joergensen, R. G., Raubuch, M. (2001b): Industrial exhaust depositions as sources of heavy metals and their long-term effects on microbial soil properties. J. Plant Nutr. Soil Sci. 164, 657–663.
10.1002/1522-2624(200112)164:6<657::AID-JPLN657>3.0.CO;2-J
CAS Web of Science® Google Scholar
Chander, K., Hartmann, G., Joergensen, R. G., Khan, K. S., Lamersdorf, N. (2008): Comparison of three methods for measuring heavy metals in soils contaminated by different sources. Arch. Agron. Soil Sci. 54, 413–422.
10.1080/03650340801927952
CAS Google Scholar
Chen, S. K., Edwards, C. A., Subler, S. (2003): The influence of two agricultural biostimulants on nitrogen transformations, microbial activity, and plant growth in soil microcosms. Soil Biol. Biochem. 35, 9–19.
10.1016/S0038-0717(02)00209-2
CAS Web of Science® Google Scholar
Docampo, R. (2006): Acidocalcisomes and Polyphosphate Granules, in J. M. Shively (ed.): Inclusions in Prokaryotes. Springer, Berlin, Germany, pp. 53–70.
10.1007/3-540-33774-1_3
Google Scholar
Docampo, R., de Souza, W., Miranda, K., Rohloff, P., Moreno, S. N. J. (2005): Acidocalcisomes? Conserved from bacteria to man. Nature Rev. Microbiol. 3, 251–261.
10.1038/nrmicro1097
CAS PubMed Web of Science® Google Scholar
Docampo, R., Ulrich, P., Moreno, S. N. (2010): Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philos. T. R. B 365, 775–784.
10.1098/rstb.2009.0179
CAS PubMed Web of Science® Google Scholar
FAO (2014): World Reference Base for Soil Resources. World Soil Resources Reports 103, FAO, Rome, Italy.
Google Scholar
Föhse, D., Claassen, N., Jungk, A. (1988): Phosphorus efficiency in plants. I. External and internal P requirement and P uptake efficiency of different plant species. Plant Soil 110, 101–109.
10.1007/BF02143545
Web of Science® Google Scholar
Gadd, G. M. (2007): Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 111, 3–49.
10.1016/j.mycres.2006.12.001
CAS PubMed Web of Science® Google Scholar
Gächter, R., Meyer, J. S. (1993): The role of microorganisms in mobilization and fixation of phosphorus in sediments. Hydrobiologia 253, 103–121.
10.1007/BF00050731
Web of Science® Google Scholar
Ghoshal, N., Singh, K. P. (1995): Effects of farmyard manure and inorganic fertilizer on the dynamics of soil microbial biomass in a tropical dryland ecosystem. Biol. Fert. Soils 19, 231–238.
10.1007/BF00336165
Web of Science® Google Scholar
Grant, W. D. (1979): Cell wall teichoic acid as a reserve phosphate source in Bacillus subtilis. J. Bacteriol. 137, 35–68.
CAS PubMed Web of Science® Google Scholar
He, Z. L., Yang, X. E., Stoffella, P. J. (2005): Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 19, 125–140.
10.1016/j.jtemb.2005.02.010
CAS PubMed Web of Science® Google Scholar
Jankowski, K. J., Budzyński, W. S., Kijewski, Ł., Klasa, A. (2014): Concentrations of copper, zinc and manganese in the roots,straw and oil cake of white mustard (Sinapis alba L.) and Indian mustard (Brassica juncea (L.) Czern. et Coss.) depending on sulphur fertilization. Plant Soil Environ. 60, 364–371.
CAS Web of Science® Google Scholar
Joergensen, R. G. (2010): Organic Matter and Micro-organisms in Tropical Soils, in P. Dion (ed.): Soil Biology and Agriculture in the Tropics. Springer, Berlin, Germany, pp. 17–44.
10.1007/978-3-642-05076-3_2
Web of Science® Google Scholar
Joergensen, R. G., Emmerling, C. (2006): Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. J. Plant Nutr. Soil Sci. 169, 295–309.
10.1002/jpln.200521941
CAS Web of Science® Google Scholar
Joergensen, R. G., Kübler, H., Meyer, B., Wolters, V. (1995): Microbial biomass phosphorus in soils of beech (Fagus sylvatica L.) forests. Biol. Fert. Soils 19, 215–219.
10.1007/BF00336162
Web of Science® Google Scholar
Kabir, A. H., Swaraz, A. M., Stangoulis, J. (2014): Zinc-deficiency resistance and biofortification in plants. J. Plant Nutr. Soil Sci. 177, 311–319.
10.1002/jpln.201300326
CAS Web of Science® Google Scholar
Kalač, P. (2010): Trace element contents in European species of wild growing edible mushrooms: a review for the period 2000–2009. Food Chem. 122, 2–15.
10.1016/j.foodchem.2010.02.045
CAS Web of Science® Google Scholar
Khan, K. S., Joergensen, R. G. (2009): Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresource Technol. 100, 303–309.
10.1016/j.biortech.2008.06.002
CAS PubMed Web of Science® Google Scholar
Khan, K. S., Joergensen, R. G. (2010): Effects of Zn and P addition on the microbial biomass in a Zn deficient calcareous soil amended with glucose. Plant Soil 335, 493–499.
10.1007/s11104-010-0442-y
CAS Web of Science® Google Scholar
Khan, K. S., Joergensen, R. G. (2012): Relationships between P fractions and the microbial biomass in soils under different land use management. Geoderma 173-174, 274–281.
10.1016/j.geoderma.2011.12.022
CAS Web of Science® Google Scholar
Khan, K. S., Chander, K., Hartmann, G., Lamersdorf, N., Joergensen, R. G. (2007): Sources of heavy metals and their long-term effects on microbial C, N and P relationships in soil. Water Air Soil Poll. 181, 225–234.
10.1007/s11270-006-9295-7
CAS Web of Science® Google Scholar
Khan, K. S., Heinze, S., Joergensen, R. G. (2009): Simultaneous measurement of S, macronutrients, and heavy metals in the soil microbial biomass with CHCl₃ fumigation and NH₄NO₃ extraction. Soil Biol. Biochem. 41, 309–314.
10.1016/j.soilbio.2008.11.001
CAS Web of Science® Google Scholar
Khan, K. S., Castillo, X., Wichern, F., Dyckmans, J., Joergensen, R. G. (2012): Interactions of mustard plants and soil microorganisms after application of sugarcane filter cake and pea residues to an Andosol. J. Plant Nutr. Soil Sci. 175, 931–938.
10.1002/jpln.201100388
CAS Web of Science® Google Scholar
Klionsky, D. J., Herman, P. K., Emr, S. D. (1990): The fungal vacuole: composition, function, and biogenesis. Microbiol. Rev. 54, 266–292.
CAS PubMed Web of Science® Google Scholar
Krpata, D., Fitz, W., Peintner, U., Langer, I., Schweiger, P. (2009): Bioconcentration of zinc and cadmium in ectomycorrhizal fungi and associated aspen trees as affected by level of pollution. Environ. Poll. 157, 280–286.
10.1016/j.envpol.2008.06.038
CAS PubMed Web of Science® Google Scholar
Loneragan, J. F., Grunes, D. L., Welch, R. M., Aduayi, E. A., Tengah, A., Lazar, V. A., Cary, E. E. (1982): Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Sci. Soc. Am. J. 46, 345–352.
10.2136/sssaj1982.03615995004600020027x
CAS Web of Science® Google Scholar
Muhammad, S., Müller, T., Mayer, J., Joergensen, R. G. (2007): Impact of growing maize (Zea mays) on the decomposition of incorporated fresh alfalfa residues. Biol. Fert. Soils 43, 399–407.
10.1007/s00374-006-0115-4
CAS Web of Science® Google Scholar
Muhammad, S., Müller, T., Joergensen, R. G. (2008): Relationships between soil biological and other soil properties in saline and alkaline arable soils from the Pakistani Punjab. J. Arid Environ. 72, 448–457.
10.1016/j.jaridenv.2007.06.016
Web of Science® Google Scholar
Nielsen, J. S., Joner, E. J., Declerck, S., Olsson, S., Jacobsen, I. (2002): Phospho-imaging as a tool for visualisation and non-invasive measurement of P transport dynamics in arbuscular mycorrhiza. New Phytol. 154, 809–819.
10.1046/j.1469-8137.2002.00412.x
CAS Web of Science® Google Scholar
Norvell, W. A., Dabkowska-Naskret, H., Cary, E. E. (1987): Effect of phosphorus and zinc fertilization on the solubility of Zn²⁺ in two alkaline soils. Soil Sci. Soc. Am. J. 51, 584–588.
10.2136/sssaj1987.03615995005100030006x
CAS Web of Science® Google Scholar
Oberson, A., Joner, E. J. (2005): Microbial Turnover of Phosphoros in Soil, in B. L. Turner (eds.): Organic Phosphorus in the Environment. CABI Publishing, Wallingford, UK, pp. 133–164.
10.1079/9780851998220.0133
Google Scholar
Płociniczak, T., Kukla, M., Wątroba, R., Piotrowska-Seget, Z. (2013): The effect of soil bioaugmentation with strains of Pseudomonas on Cd, Zn and Cu uptake by Sinapis alba L. Chemosphere 91, 1332–1337.
10.1016/j.chemosphere.2013.03.008
CAS PubMed Web of Science® Google Scholar
Quintern, M., Lein, M., Joergensen, R. G. (2006): Changes in soil biological quality indices after long-term addition of shredded shrubs and biogenic waste compost. J. Plant Nutr. Soil Sci. 169, 488–493.
10.1002/jpln.200521801
CAS Web of Science® Google Scholar
Sadeghzadeh, B., Rengel, Z. (2011): Zinc in Soils and Crop Nutrition, in M. J. Hawkesford (eds.): The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops. Wiley-Blackwell, Oxford, UK, pp. 335–375.
10.1002/9780470960707.ch16
Google Scholar
Salamanca, E. F., Raubuch, M., Joergensen, R. G. (2006): Microbial reaction of secondary tropical forest soils to the addition of leaf litter. Appl. Soil Ecol. 31, 53–61.
10.1016/j.apsoil.2005.04.005
Web of Science® Google Scholar
Tu, C., Zheng, C. R., Chen, H. M. (2002): Effect of heavy metals on phosphorus retention by Typic Udic Ferrisols: equilibrium and kinetics. Pedosphere 12, 15–24.
CAS Google Scholar
Tyler, G. (1980): Metals in sporophores of basidiomycetes. T. Brit. Mycol. Soc. 74, 41–49.
10.1016/S0007-1536(80)80005-2
CAS Web of Science® Google Scholar
Vance, E. D., Brookes, P. C., Jenkinson, D. S. (1987): An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707.
10.1016/0038-0717(87)90052-6
CAS Web of Science® Google Scholar
Wallander, H., Mahmood, S., Hagerberg, D., Johansson, L., Pallon, J. (2003): Elemental composition of ectomycorrhizal mycelia identified by PCR-RFLP analysis and grown in contact with apatite or wood ash in forest soil. FEMS Microbiol. Ecol. 44, 57–65.
10.1111/j.1574-6941.2003.tb01090.x
CAS PubMed Web of Science® Google Scholar
Wang, J. J., Harrell, D. L. (2005): Effect of ammonium, potassium, and sodium cations and phosphate, nitrate, and chloride anions on zinc sorption and lability in selected acid and calcareous soils. Soil Sci. Soc. Am. J. 69, 1036–1046.
10.2136/sssaj2004.0148
CAS Web of Science® Google Scholar
Watts-Williams, S. J., Turney, T. W., Patti, A. F., Cavagnaro, T. R. (2014): Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant Soil 384, 79–92.
10.1007/s11104-014-2140-7
CAS Web of Science® Google Scholar
White, C., Gadd, G. M. (1987): The uptake and cellular distribution of zinc in Saccharomyces cerevisiae. J. Gen. Microbiol. 133, 727–737.
Web of Science® Google Scholar
Wu, J., Joergensen, R. G., Pommerening, B., Chaussod, R., Brookes, P. C. (1990): Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biol. Biochem. 22, 1167–1169.
10.1016/0038-0717(90)90046-3
CAS Web of Science® Google Scholar
Zhao, K., Selim, H. M. (2010): Adsorption-desorption kinetics of Zn in soils: influence of phosphate. Soil Sci. 175, 145–153.
10.1097/SS.0b013e3181dd51a0
CAS Web of Science® Google Scholar
Zhang, Y. Q., Deng, Y., Chen, R. Y., Cui, Z. L., Chen, X. P., Yost, R., Zhang, F. S., Zou, C. Q. (2012): The reduction in zinc concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar zinc application. Plant Soil 361, 143–152.
10.1007/s11104-012-1238-z
CAS Web of Science® Google Scholar
Zalewska, M., Nogalska, A. (2014): Phytoextraction potential of sunflower and white mustard plants in zinc-contaminated soil. Chil. J. of Agric. Res. 74, 485–489.
10.4067/S0718-58392014000400016
Web of Science® Google Scholar

Citing Literature

Volume178, Issue6

December, 2015

Pages 834-840

Response of white mustard (Sinapis alba) and the soil microbial biomass to P and Zn addition in a greenhouse pot experiment

Abstract

1 Introduction