Molybdenum in the Environment

Molybdenum in the Biosphere

Molybdenum in plants

Molybdenum is an essential micronutrient for plant growth and for microsymbionts. Even when the total Mo content of the soil is sufficient, since Mo is often sequestered by Fe- or Al-oxohydroxides, especially in acidic soils, the concentration of the water-soluble molybdate anion available for uptake by plants may be limiting for the plant. No specific molybdenum uptake system is known for plants, but since molybdate and sulfate behave similarly and have similar structure, uptake of molybdate could be mediated unspecifically by one of the sulfate pathways.

Zimmer, W, Mendel, R, Molybdenum metabolism in plants, Plant Biology, 999,1, 160-168.

Molybdenum concentrations in various plants

Molybdenum Concentrations in Plants [1]

Source

Concentration /ppm dry weight

Land Plants

0.9

Plankton

1.0

Brown Algae

0.45

Bryophytes

0.7

Ferns

0.8

Gymnosperms

0.13

Angiosperms

0.9

Fungi

1.5

hay [2]

0.78

citrus leaves [2]

0.14

[1] Bowen, H. J. M., Trace Elements in Biochemistry, 1966, Academic Press, N. Y.
[2] Alonso, J.I.G., Camblor, M.G., Bayon, M.M., Marchante Gayon, J.M., Sanz Medel, A., Different quantification approaches for the analysis of biological and environmental samples using inductively coupled plasma mass spectrometry, Journal Of Mass Spectrometry, 1997, 32, 556-564.

Tobacco 0.3 – 1.76 microg Mo/g

Voss, R.C., Nicol, H., Metallic trace elements in tobacco, Lancet, 1960, 2, 435 – 436.

Concentrations of barium (Ba), calcium (Ca), Cu, iron (Fe), K, magnesium (Mg), manganese (Mn), molybdenum (Mo), sodium (Na), rubidium (Rb), strontium (Sr), and zinc (Zn) in leaf and stem tissues were correlated with treatment and tissue. Generally, increasing Cu resulted in elevated Ba, Fe, Mo, and Sr as well as Cu levels.
The presence of peat resulted in reduced levels, generally in both leaf and stem, of Ba, Mg, Mn, Rb, and Zn and increased levels of Fe, K, and Mo.


Elemental concentrations were higher in leaf tissue rather than stem, with the exceptions of Na and Zn.
Elemental concentration ranges, over all tissues and conditions of added Cu and peat were (mg kg-1) Ba 9-49, Ca 6380-16340, Cu 2-11, Fe 10-57, K 4070-16950, Mg 900-4260, Mn 22-197, Mo 0.02-0.19, Na 28-124, Rb 0.7-12, Sr 41-58, Zn 18-48

Ihnat, M., Neilsen, G. H., and Hogue, E. J., Elemental content relationships in greenhouse grown apple seedlings supplemented with copper and peat, Communications in Soil Science and Plant Analysis, 2000, 31, 803-825.

Tropical grasses

Mo 0.02-1.23 mg kg-l dry matter

Youssef, F.G., McDowell, L.R., Brathwaite, R.A.I., The status of certain trace minerals and sulphur of some tropical grasses in Trinidad, Tropical Agriculture, 1999, 76, 57-62.

Molybdenum in plants uptake and accumulation

Molybdenum is utilized by selected enzymes to carry out redox reactions. Enzymes that require molybdenum for activity include nitrate reductase, xanthine dehydrogenase, aldehyde oxidase and sulfite oxidase. Loss of Mo-dependent enzyme activity (directly or indirectly through low internal molybdenum levels) impacts upon plant development, in particular, those processes involving nitrogen metabolism and the synthesis of the phytohormones abscisic acid and indole-3 butyric acid. It is unclear how plants access molybdate from the soil solution or later redistribute it once in the plant. Plants have similar physiological molybdenum transport phenotypes to those found in prokaryotic systems. Analysis of prokaryotic molybdate transport mechanisms and anion transport mechanisms in plants will help our understanding of how molybenum is accumulated.

Kaiser, B.N., Gridley, K. L., Brady, J. N., Phillips, T., and Tyerman, S. D., The role of molybdenum in agricultural plant production, Annals of Botany, 2005, 96, 745-754.
Molybdenum concentration varies with location and species: for example, in pastures in different areas molybdenum concentrations varying from 0.1 to 200 ppm dry weight have been reported [Underwood, 1962; Kolomiitseva et al., 1970].
Underwood, E. J., Trace Elements in Human and Animal Nutrition, 2nd Ed. 1962, 100. Academic Press, London.
Kolomiitseva, M. G., Polonskaya, M. N. and Osipov, G. K.,Mikroelem. Sel. Khoz. Med., 1968, 4, 183;
Warren, H . V., Delavault, R. E., Fletcher, K. W., Geology Environ. Contr. Bull., 1971, 6, 34.
U.S Department of the Interior, 1967, 1968, 1970
Sequi, P., Agrochimica, 1972 (Publ. 1973), 17, 119
Webb, J. S., Geol. Soc. Amer., Mem., 1971, 123, 31.
Ivanova, N. N., Agrochimica, 1972 (Publ. 1973), 17, 96.

Mo in plants grown on a landfill site

The mean concentrations (microg/g dry weight) of Se and Mo in the shoots of plants grown on a landfill site did not exceed, respectively,
0.12 (Se) and 18.7 (Mo) in bird's-foot trefoil (Lotus corniculatus L.),
0.06 and 12.1 in red clover (Trifolium pratense L.),
0.07 and 5.3 in timothy (Phleum pratense L.),
0.09 and 2.2 in a mixture of grasses.
These concentrations were greater than those in the same species harvested concurrently from a non-landfill site.

Molybdenum uptake in plants

The uptake of Mo is induced by NO3- and inhibited by sulfate.

W. Reid, R.J., Mechanisms of micronutrient uptake in plants, Australian Journal of Plant Physiology, 2001, 28, 659-666.

When supplied with molybdate Indian mustard (Brassica juncea) seedlings accumulated water-soluble blue crystals in their peripheral cell lavers. A mutant without anthocyanin did not show accumulation of a blue molybdenum compound. Mo appears to be sequestered in vacuoles of the peripheral cell layers of Brassica spp. as a blue compound, probably a Mo-anthocyanin complex.

Hale, K.L., McGrath, S. P., Lombi, E., Stack, S. M., Terry, N., Pickering, I. J., George, G. N., and Pilon-Smits, E. A. H., Molybdenum sequestration in Brassica species. A role for anthocyanins?, Plant Physiology, 2001, 126, 1391-1402.

Molybdate cellular transport

For molybdoenzymes synthesis, e.g. nitrogenase, molybdenum as molybdate must be transported inside the cell. In Bradyrhizobium japonicum, the modABC genes code for a high-affinity ABC-type molybdate transporter.

The effect of inoculation of soybean plants with strains affected in the molybdate transport was investigated with the modA and modB mutants, unable to grow in culture media under molybdate-deficient conditions.

When soybean plants were inoculated with one of these strains and grown in a molybdate-deficient mineral solution the nodulation was not affected, but the nitrogen-fixing ability of the mod mutants was impaired.

Addition of molybdate to the nutrient mineral solution used for plant growth restored the wild-type phenotype.

The amount of molybdate required for supression of the mutant phenotype was dependent on sulfate concentration. The molybdate concentration required for the functioning of the mutant strains was greater when the medium was supplemented with high amounts of sulfate.

There exists in B. japonicum, at least, three independent molybdate transport systems: a high-affinity transporter encoded by the modABC genes, a low affinity system corresponding to a sulfate transporter, and a third transporter that would be functional in the presence of high sulfate concentrations.

Tresierra-Ayala, A., Delgado, M. J., Guzman, R. A., Rengifo, A. L., and Bedmar, E. J., Molybdate Transport in the Bradyrhizobium Japonicum - Glycine Max L. Symbiosis, Journal of Soil Science and Plant Nutrition, 2011, 11, 8-17.

Molybdenum and trace element concentrations in red and white cabbage

Cabbage (Brassica oleracea) is a vegetable food that is found in red and white varieties, and consumed worldwide raw or cooked. The mineral composition of cabbage collected in 24 Brazilian cities was determined and the results were evaluated using multivariate analysis. The samples (31 white, 24 red) were digested with nitric acid and hydrogen peroxide and analyzed with inductively coupled plasma optical emission spectrometry. The accuracy of the method was confirmed by analysis of a certified reference material of spinach leaves, from the National Institute of Standard and Technology. Element concentrations (mg element/kg sample) were: potassium, 1602.9 to 4068.3; phosphorus, 217.5 to 766.2; calcium, 221.9 to 744.7; magnesium, 67.2 to 286.0; manganese, 0.81 to 4.40; iron, 1.91 to 8.60; molybdenum, 0.01 to 0.24; zinc, 1.17 to 5.10; sodium, 27.2 to 591.0; strontium, 0.35 to 5.79. The mineral composition of the red species was not different from the white species.

Anunciacao, D. S., Leao, D. J., de Jesus, R. M., and Ferreira, S. L. C., Use of Multivariate Analysis Techniques for Evaluation of Analytical Data-Determination of the Mineral Composition of Cabbage (Brassica oleracea), Food Analytical Methods, 2011, 4, 286-292.


Mo absorption by cress

Mo is readily absorbed both into cress (Lepidium sativum) and into french beans (Phaseolus vulg. var. nanus) [Giussani et al., 1998]. For cress grown from seeds in Petri dishes on blotter paper moistened with tap water solutions of molybdate of different concentrations, the Mo content increased linearly with time before harvesting and with the molybdate concentration.

Giussani, A., Heinrichs, U., Roth, P., Werner, E., Schramel, P., Wendler, A., Biokinetic studies in humans with stable isotopes as tracers. Part 1: A methodology for incorporation of trace metals into vegetables, Isotopes In Environmental And Health Studies, 1998, 34,291-296.

Mo in sugarcane leaves

In crops of the sugarcane, the concentrations of molybdenum (Mo) in the leaves are generally lower than 0.3 mg Mo kg-1 . These low concentrations have resulted in limitations in the methods and instruments that can be used for these analyses. The objective of this study was to evaluate three different techniques to determine the concentration of Mo in sugarcane leaves sampled in the principal sugarcane-producing areas in Brazil. Two spectrometric techniques were evaluated by using ICP-EAS (Inductively Coupled Plasma-Emission Automated System) and DCP-MEAS (Direct Coupled Plasma-Multiple Emission Automated System) and a colorimetric technique of the reaction between potassium iodide and hydrogen peroxide (KI-H2O2). The techniques ICP-EAS and KI-H2O2 produced results of satisfactory accuracy and precision, whereas the DCP-MEAS consistently overestimated the Mo concentrations in cane leaves. The KI-H2O2 technique showed sensitivity 5 times greater than the ICP-EAS, with minimum detection limits of 0.1 and 0.5 mg Mo kg-1 , respectively

Polidoro, J. C., Medeiros, A. F. A., Xavier, R. P., Medeiros, J. A., Boddey, R. M., Alves, B. J. R., and Urquiaga, S., Evaluation of techniques for determination of molybdenum in sugarcane leaves, Communications in Soil Science and Plant Analysis, 2006, 37, 77-91.

Lettuce – yield increased by fertilisation with molybdenum and nitrogen

The aim was to evaluate the influence of nitrogen and molybdenum doses on the yield and contents of macronutrients in crisphead lettuce (Lactuca sativa L.). The experiment was carried out in the town of Tres Pontas, State of Minas Gerais, Brazil, from October to December, 2002.

The treatments combined nitrogen doses in the top dressing additional to the 60 kg/ha N dose applied by the agriculturist (0.0, 60.0, 120.0, and 180.0 kg/ha) and five foliar molybdenum doses (0.0, 35.1, 70.2, 105.3, and 140.4 g/ha).

The largest commercial fresh mass was obtained with the dose of 89.1 kg/ha nitrogen in the top dressing and 94.2 g/ha molybdenum.

With increasing doses of nitrogen and molybdenum

  • the levels of N and P increased
  • the levels of potassium decreased
  • the levels of Ca, Mg and S increased in the plant tops.
de Resende, G. M., Alvarenga, M. A. R., Yuri, J. E., de Souza, R. J., Mota, J. H., de Carvalho, J. G., and Rodrigues, J. C., Yield and content of macronutrients in crisphead lettuce (Lactuca sativa L.) in the summer planting as a function of nitrogen and molybdenum doses, Ciencia e Agrotecnologia, 2009, 33, 153-163.

Plants lettuce accumulation of molybdenum in plants and soils following amendments of Mo compost

A limit for molybdenum loading of soil developed from compost additions is proposed as 55 mg Mo/ kg soil, a value which is presently greater than the Canadian Council for Ministers of the Environment (CCME) Guidelines for the use of type B compost in Canada

The growth of lettuce (Lactuca sativa L.) and barley (Hordeum vulgar) and accumulation of molybdenum in plants and soils were evaluated in a pot experiment following amendments of molybdenum compost (1.0 g/ kg) to a Truro sandy loam.

Dry-matter yield: up to 25% molybdenum compost, no effect; at the 50% compost treatment dry-matter yield decreased.

pH: 50% compost treatments, soil pH increased an average of 0.5 units.

Extractable molybdenum:

50% compost treatments:

in the growth medium increased the nitric acid extractable molybdenum to 150 mg/ kg and diethylenetriaminepentaacetic acid extractable molybdenum to 100 mg/ kg;

tissue Mo concentration to 569 and 478 mg/ kg in the lettuce and barley.

25% compost treatment:

in the growth medium produced about 55 mg/ kg of total molybdenum;

tissue Mo concentration of 348 mg/ kg in lettuce and 274 mg/ kg in barley without any phytotoxicity.

Kashem, M. A. and Warman, P. R., Effect of High-Molybdenum Compost on Soils and the Growth of Lettuce and Barley, Communications in Soil Science and Plant Analysis, 2009, 40, 2225-2233.

Plants agriculture seed treatment

Molybdenum was applied as a concentrated suspension of molybdenum trioxide in water to soybean seeds resulting in in higher soybean yields than in a control.

Lana, R. M. Q., de Faria, M. V., Bonotto, I., and Lana, A. M. Q., Cobalt and Molybdenum Concentrated Suspension for Soybean Seed Treatment, Revista Brasileira de Ciencia do Solo, 2009, 33, 1715-1720.

Influence of Salinity on the Nitrogen Metabolism of Cordyline fruticosa

The aim was to study the influence of irrigation water salinity on the nitrogen metabolism of Cordyline fruticosa var. 'Red Edge'.

Irrigated agriculture depends on adequate and quality water supplies. As the level of salt increases in an irrigation source, the quality of that water for plant growth decreases. Crop plants are usually nonhalophytes that tolerate only moderate salt concentrations. Under salinity, they accumulate salt in their aboveground organs and, to a smaller extent, in roots. High salinity reduces plant growth and leaf area, which prejudices quality, especially in ornamental crops. The study of the behavior of ornamental plants that are tolerant to saline waters can be an advantage in areas with poor quality waters.

Four nutrient solutions with different electrical conductivity levels were applied by adding sodium chloride to the irrigation water. As salinity increases, nitrogen concentration increases in the roots but not the leaves. In leaves, nitrate reductase in vivo activity declines when salinity increases; when a substrate, nitrate, or a cofactor, molybdenum, is added, nitrate reductase activity increases. Potential nitrate reductase activity shows no differences between treatments; nitrate reductase synthesis is not affected by salinity. So, the diminution of the nitrate reductase in vivo activity suggests a nitrate and molybdenum level metabolic imbalance. In roots, molybdenum is more restrictive of the nitrate reductase activity than the nitrate substrate level. There are more amino acids in T1 than in T4, but it seems that there are no significant differences in T2 and T3. No significant differences are observed in the protein content; this indicates that amino acid diminution is due to the maintenance of the protein content. In conclusion, it can be said that the increased activity of nitrate reductase in roots may constitute part of an adaptation strategy of the plant to an increasing salinity in the growing medium

Plaza, B. M., Jimenez, S., Segura, M. L., Contreras, J. I., and Lao, M. T., Influence of Salinity on the Nitrogen Metabolism of Cordyline fruticosa, Communications in Soil Science and Plant Analysis, 2009, 40, 462-472.

Molybdenum in plants - molybdenum and phosphorus interaction photosynthesis and grain yield of Brassica napus

A pot experiment with acid yellow-brown soil was conducted to investigate the interactive effects of molybdenum and phosphorus fertilizers on the photosynthetic characteristics of seedlings and grain yield of Brassica napus which is sensitive to soil P and Mo deficiency.

Both Mo and P fertilizers were applied at three levels (mg kg-1 soil):

Mo: 0, 0.15, 0.30

P: 0, 80, 160 .

P fertilizer application in the absence or presence of Mo fertilizer increased

grain yield,

soluble sugar concentrations of seedling leaves,

DM and P accumulation of seedling shoots of Brassica napus.

Mo fertilizer increased these parameters only in the presence of P fertilizer.

Mo accumulation in shoots, chlorophyll concentrations and net photosynthesis rate (P (n)) of seedling leaves were increased by both Mo and P fertilizers, particularly with the combination of the two fertilizers.

the Mo and P fertilizers increased photosynthetic rate through two different mechanisms, with Mo increasing photosynthetic activity of mesophyll cells, and P increasing stomatal conductance.

There was a synergetic effect on photosynthesis and grain yield between Mo and P fertilizers and it is beneficial for Brassica napus growth to co-apply both the Mo and P fertilizers

Liu, H. G., Hu, C. X., Sun, X. C., Tan, Q. L., Nie, Z. J., and Hu, X. M., Interactive effects of molybdenum and phosphorus fertilizers on photosynthetic characteristics of seedlings and grain yield of Brassica napus, Plant and Soil, 2010, 326, 345-353.

Rye flour and rye

Trace Elements Species including molybdenum fractionation in Rye Flour and Rye

The fractionation of Cd, Cu, Mo, Ni, and Zn species in extracts of rye (cv. Fernando) seedlings and rye flour was performed by SEC/ICP-MS method. The majority of Cu, Zn, and Ni in all samples were bound in the 1-2 kDa fraction. Molybdenum occurred in all samples in the fraction of 3 kDa.

Polak, J., Mestek, O., Koplik, R., Santrucek, J., Kominkova, J., and Kodicek, M., Trace Elements Species Fractionation in Rye Flour and Rye (Secale cereale L.) Seedlings, Czech Journal of Food Sciences, 2009, 27, 39-48.

Plants alfalfa

Alfalfa crops were grown in the field at the University of Ankara over two seasons between 2001 and 2003 with sulfur supplied as gypsum at rates of 0 (control), 160 (S1), and 240 (S2) kg /ha. Sulfur fertilization increased sulfur concentrations and improved alfalfa hay yield for both years. Molybdenum concentration of the alfalfa was significantly reduced by S1 treatment in year 1. Applied S had no effect on copper.

Gunes, A., Inal, A., Pilbeam, D. J., and Kadioglu, Y. K., Effect of Sulfur on the Yield and Essential and Nonessential Element Composition of Alfalfa Determined by Polarized Energy Dispersive X-ray Fluorescence, Communications in Soil Science and Plant Analysis, 2009, 40, 2264-2284.

Plants rice beneficial effect of molybdenum and nickel interaction on plant growth

This is the first evidence for a beneficial effect of molybdenum and nickel interaction on plant growth. Upland rice plants, cultivar 'IAC 202,' were grown in nutrient solution until full tillering. Treatments consisted of ammonium nitrate or urea as nitrogen source plus molybdenum and/or nickel.

Moraes, M. F., Reis, A. R., Moraes, L. A. C., Lavres, J., Vivian, R., Cabral, C. P., and Malavolta, E., Effects of Molybdenum, Nickel, and Nitrogen Sources on the Mineral Nutrition and Growth of Rice Plants,




Forests

Nitrate reductase activity in two temperate forests - effects of elevated carbon dioxide and nitrogen fertilization

The effects of elevated CO2 and nitrogen availability on the activity of nitrate reductase, the enzyme catalyzing the reduction of nitrate to nitrite, are reported in two temperate forests-a closed canopy sweetgum (Liquidambar styraciflua) plantation in Tennessee (Oak Ridge National Laboratory) and a loblolly pine (Pinus taeda) stand in North Carolina (Duke). Both CO2 and nitrogen enrichment had species specific impacts on nitrate reductase activity. Elevated CO2 and nitrogen fertilization decreased foliar nitrate reductase activity in P. taeda, but there were no treatment effects on L. styraciflua nitrate reductase activity at Oak Ridge National Laboratory or Duke. Nitrate reductase activity in 1-year P. taeda needles was greater than in 0-year old needles across treatments. P. taeda nitrate reductase activity was negatively correlated with bio-available molybdenum concentrations in soils; CO2 and nitrogen-mediated changes in soil nutrient status may be altering soil-plant nitrogen-dynamics. The variation in response among species may reflect different strategies for acquiring nitrogen; elevated CO2 may alter plant nitrogen dynamics through changes in nitrate reductase activity.

Nitrogen availability limits plant production in many terrestrial ecosystems and is a key regulator of plant response to elevated CO2. Plant nitrogen status is a function of both soil nitrogen availability and plant nitrogen uptake and assimilation capacity. As a rate-limiting step in nitrate assimilation, the reduction of nitrate is an important component of plant physiological response to elevated CO2 and terrestrial carbon sequestration.

Natali, S., Sanudo-Wilhelmy, S. A., and Lerdau, M., Effects of elevated carbon dioxide and nitrogen fertilization on nitrate reductase activity in sweetgum and loblolly pine trees in two temperate forests, Plant and Soil, 2009, 314, 197-210.

Nitrogen fixation in tropical forests - increased by molybdenum addition to soil

Nitrogen fixation, the biological conversion of dinitrogen to plant-available ammonium, requires the enzyme nitrogenise of which molybdenum is a co-factor. Nitrogen fixation is the primary natural input of nitrogen to ecosystems(1), and influences plant growth and carbon exchange at local to global scales(2-6). The role of nitrogen fixation in tropical forests is of particular concern, as tropical forest ecosystems harbour abundant nitrogen-fixing organisms(1,4) and represent one third of terrestrial primary production(4,7,8).

Molybdenum is shown to limit nitrogen fixation by free-living heterotrophic bacteria in soils of lowland Panamanian forests. The nitrogen fixation response to long-term nutrient manipulations in intact forests, and to short-term manipulations in soil microcosms was measured. Nitrogen fixation increased sharply in treatments of molybdenum alone, in micronutrient treatments that included molybdenum by design and in treatments with commercial phosphorus fertilizer, in which molybdenum was a contaminant. Nitrogen fixation did not respond to additions of phosphorus that were not contaminated by molybdenum.

Molybdenum alone can limit asymbiotic nitrogen fixation in tropical forests. Molybdenum limitation may be common in highly weathered acidic soils, and may constrain the ability of some forests to acquire new nitrogen in response to CO2 fertilization(9)

1.Galloway, J. N. et al. Nitrogen cycles: Past, present, and future. Biogeochemistry70, 153–226 (2004).

2.Mahaffey, C., Michaels, A. F. & Capone, D. G. The conundrum of marine N2 fixation. Am. J. Sci. 305, 546–595 (2005).

3.Vitousek, P. M. et al. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45 (2002).

4.Cleveland, C. C. et al. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob. Biogeochem. Cycles 13, 623–645 (1999).

5.Reich, P. B., Hungate, B. A. & Luo, Y. Q. Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu. Rev. Ecol. Evol. Syst. 37, 611–636 (2006).

6.Gutschick, V. P. Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118, 607–637 (1981).

7.Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

8.Clark, D. A. Detecting tropical forests' responses to global climatic and atmospheric change: Current challenges and a way forward. Biotropica 39, 4–19 (2007).

9.Hungate, B. A. et al. CO2 elicits long-term decline in nitrogen fixation. Science 304, 1291–1291 (2004).

Barron, A. R., Wurzburger, N., Bellenger, J. P., Wright, S. J., Kraepiel, A. M. L., and Hedin, L. O., Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils, Nature Geoscience, 2009, 2, 42-45.

Molybdenum uptake and transport in plants

The molybdenum concentration in the sap was approximately 11 times greater in the absence of sulfate in the nutrient medium. Restoring sulfate to the nutrient medium without sulfur depressed the Mo concentration of the sap at the next harvest to a value similar to that in plants receiving sulfate from the onset of the growth period and, similarly, raised the S concentration as well. Sulfate and molybdate compete for the same carrier and transport sites in uptake, and sulfate deficiency leads to excess Mo uptake.

Alhendawi, R.A., Kirkby, E. A., and Pilbeam, D. J., Evidence that sulfur deficiency enhances molybdenum transport in xylem sap of tomato plants, Journal of Plant Nutrition, 2005, 28, 1347-1353.

Molybdate transport in plants

A molybdate transporter, ‘MOT1’, has been identified from the plant Arabidopsis thaliana. The following is a summary of the paper. The reader is recommended to consult the original paper and key references for methods and justifications.

MOT1 is expressed in both roots and shoots. The MOT1 protein is localized, in part, to plasma membranes and to vesicles. MOT1 enhances molybdate uptake from soil into root cells for utilization and also for translocation to shoots. MOT1 is required for efficient uptake and translocation of molybdate and for normal growth under conditions of limited molybdate supply. MOT1 is a high-affinity Mo transporter. The high molybdate affinity of MOT1 enables plants to obtain scarce molybdate from soil.

MOT1 is also specific for molybdate (as opposed to sulfate).

The affinity of MOT1 for molybdate was determined from kinetic studies in yeast of uptake of molybdate (applied as ammonium heptamolybdate) vs time. For time-course analysis of molybdate uptake, cells were transferred to the medium supplemented with 24 nM ammonium heptamolybdate, and shaken at 30°C for 0, 5, 10, 15, 20, 30, 45, or 60 min. For kinetic analysis of molybdate uptake cells were transferred to the medium supplemented with 7, 8, 10, 12, 16, 24, 97 or 194 nM ammonium heptamolybdate, and shaken at 30 °C for 15 min.

The stationary level of molybdenum concentration in cells expressing MOT1 was roughly 30 microM; more than 100-fold higher than that in the medium used for the uptake study. Thus MOT1 is a molybdate transporter capable of transporting molybdate against a concentration gradient.

Analysis of the kinetics of molybdate uptake (Lineweaver–Burk plot) by yeast expressing MOT1 gave Km 21 ± 4 nM and Vmax 0.5 ±0.1 microg_g-1DW min-1 where Km, the Michaelis constant, is the dissociation constant of a MOT1-molybdate complex and Vmax is the maximal uptake velocity. The authors comment that 20 nM is the lowest reported Km value of the mineral–nutrient transporters in plants.

So MOT1 is well described as a high-affinity molybdate transporter.

The genetic mechanism that controls Mo concentration in Arabidopsis thaliana shoots, was studied in detail. The trait is mostly regulated by a single locus on chromosome 2 in a region containing a gene (At2g25680) annotated as Sultr5;2 (representing a member of the sulfate transporter group). At2g25680 was identified as a molybdate transporter by studying the molybdate uptake of Arabidopsis thaliana mutant lines (mot1-1 and mot1-2 having modified At2g25680) grown in the presence of 170 nM molybdate for five weeks, after which the molybdenum concentrations in shoots and roots were determined. The molybdenum concentrations in shoots of the mot1-1 and mot1-2 mutant plants were reduced to 10% and 20% of that in the wild type, and, in roots, the molybdenum concentrations were reduced to 20% and 25% of that in the wild type. Thus At2g25680 (named MOT1) is the determinant of the Mo concentration in both roots and shoots.

Tomatsu, H., Takano, J., Takahashi, H., Watanabe-Takahashi, A., Shibagaki, N., and Fujiwara, T., An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil, Proceedings of the National Academy of Sciences of the United States of America, 2007, 104, 18807-18812.

Uptake of elements including molybdenum by Lotus Japonicus

Lotus japonicus was used to study the distribution and interconnections of 15 elements in plant tissues, including essential and non-essential elements: boron (B), sodium (Na), magnesium (Mg), potassium (K), calcium (Ca), manganese (Mn), iron (Fe), nickel (Ni), copper (Cu), zinc (Zn), arsenic (As), strontium (Sr), molybdenum (Mo), cadmium (Cd) and cesium (Cs). Large amounts of B and Ca accumulated in plant leaves, while Fe, Na, Ni, As and Cd tended to mainly occur in the roots, and Mo was the only element to accumulate in the stems. The elemental compositions within plants were severely disturbed by treatment with toxic elements. Competition between element pairs in the same group (e.g. K and Cs; Ca and Sr) was not found. Iron, Cu and Zn accumulation were induced by Cd and Ni addition. When natural variants grew in a nutrition solution with subtoxic levels of As, Cd, Cs, Ni, Mo and Sr, intriguing relationships between the elements (such as Fe, As and K; Mg and Ni; Mn and Ca) were revealed using principal-component analysis. This study on the plant ionome offers detailed information of element interactions and indicates that chemically different elements might be closely linked in uptake or translocation systems

Chen, Z., Watanabe, T., Shinano, T., Ezawa, T., Wasaki, J., Kimura, K., Osaki, M., and Zhu, Y. G., Element interconnections in Lotus japonicus: A systematic study of the effects of element additions on different natural variants, Soil Science and Plant Nutrition, 2009, 55, 91-101.


Molybdate and selenate alter sulfate transport and assimilation in Brassica

The interaction of selenate and molybdate with the transport and assimilation of sulfate, and the effect of sulfur on selenium and molybdenum accumulation were investigated in Brassica juncea. Plants were supplied with different combinations of sulfur and selenium, or sulfur and molybdenum for 24 h, and selenate and molybdate were given to plants at concentrations (200 microM) equal to that of sulfate in the sulfur -sufficient condition.

Selenium and molybdenum significantly reduced the plant growth. In sulfur -sufficient plants, selenium and molybdenum decreased sulfate uptake rate (at 24 h), and selenium repressed the expression of the sulfate transporter BjSultr2.1. This effect was different from the one observed for sulfate, which rapidly inhibited the sulfate uptake rates in + sulfur plants.

In sulfur -starved plants, selenium. molybdenum and sulfur repressed sulfate uptake immediately (after 10 min), and the concomitant down-regulation of BjSultr2.1 occurred only in roots of plants treated with sulfur. In plants exposed to selenium or molybdenum the root expression of BjSultr2.1 was repressed later, after 6 h.

Sulfur -starved plants accumulated significantly more selenium and molybdenum than sulfur -sufficient plants, likely due to the lack of competition of molybdate or selenate with sulfate for the transport through the same carriers. The up-regulation of the molybdenum transporter (MOT1) gene expression could explain the higher amount of molybdenum than selenium measured in the plant tissues.

Selenium and molybdenum reduced the levels of cysteine (Cys) and glutathione (GSH) in + sulfur plants, but increased the amount of these non-protein thiols in - sulfur plants. The increase of GSH content in - sulfur + selenium plants was likely responsible for the down-regulation of the selenium binding protein (SBP1) gene, while the induction of SBP1 observed in + sulfur plants was mainly due to selenium toxicity. The up-regulation of SBP1 was also evidenced in plants exposed to molybdenum, regardless of sulfur availability and GSH content.

The results give better insight into plant uptake mechanisms for selenium and molybdenum, and also have implications for phytoremediation. The interactions between sulfate and selenate or molybdate must be carefully considered when plants are employed for the remediation of selenium - or molybdenum -contaminated sites, as the accumulation of the two contaminants in plants might be altered by the sulfate concentration in the growing medium.

Schiavon, M., Pittarello, M., Pilon-Smits, E. A. H., Wirtz, M., Hell, R., Malagoli, M.Selenate and molybdate alter sulfate transport and assimilation in Brassica juncea L. Czern.: Implications for phytoremediationEnvironmental and Experimental Botany, 2011,75, 41-51.

Molybdenum in pastures and herbage

Pasture

Concentrations in normal herbage may range from 0.1 to 0.3 ppm on a dry matter basis. The molybdenum is present as soluble ammonium molybdate, insoluble molybdenum trioxide, calcium molybdate and molybdenum disulfide. In areas of high industrial activity herbage values of up to 231 ppm have resulted. The differential in the molybdenum concentration of soils due to pH could result in differing levels due to the consumption of herbage grown in soils of regional type.

Gardner, A. W. and Hall-Patch, P. K., J. Nutr. , 1962, 84, 31.

Some soils may require supplemental molybdenum. These include soils low in organic matter, severely eroded or heavily weathered soils, soils low in total molybdenum, sandy soils, soils high in iron, and acid soils (pH <6.3). Molybdenum is not readily absorbed by plants from acid soils and liming or addition of molybdenum is required to increase the molybdenum concentration in pasture. Some plants exhibit visual symptoms of molybdenum deficiency, e.g., the classic whiptail in cauliflower and yellow spot in citrus, but often visual symptoms of molybdenum deficiency are not present or appear as symptoms of nitrogen deficiency. A typical supplemental molybdenum addition for legumes is approximately 0.25 kg molybdenum per acre. Molybdenum can be applied in fertilisers, by seed treatment or foliar sprays.

Some pastures have exceptionally high concentrations of molybdenum (generally associated with alkaline soils), and may give rise to symptoms of molybdenum toxicity in sheep and cattle. Guideline values of up to 50 mg/kg dry weight have been fixed for molybdenum concentrations in agricultural soils [Hornick et al., 1977]. A higher incidence of uratic diathesis was reported from a locality in Armenia where the soil was found to contain 77 mg/kg of molybdenum and 39 mg/kg of copper. The total daily intake of molybdenum and copper in the adults of this area were estimated to be 10 times that of an adult in a control area [Kovalskij et al., 1961; ILO Geneva, 1980].

Hornick, S. B., Baker, D. E. and Guss, S. B., Molybdenum in the Environment, 1977, 2, Marcel Dekker, New York.
Kovalskij, V. V., Jarovaja, G. A. and Smavonjan, D. M., Z. Obsc. Biol., 1961, XII, 179.
ILO Geneva, 1980.

Serum and liver concentrations of copper, iron, zinc and molybdenum in goats and sheep

Serum and liver concentrations were measured of copper, iron, zinc and molybdenum in sheep and goats slaughtered in the semiarid region of the state of Pernambuco, northeastern Brazil, during the rainy and dry seasons to establish if copper deficiency which occurs in the region is primary, or secondary to high levels of molybdenum and/or iron.

Low copper concentrations are not related with high molybdenum ingestion.

Serum and liver samples from 141 goats and 141 sheep were digested in nitric-perchloric acid and analyzed by coupled plasma atomic absorption spectrophotometry (ICPOES).

Based on copper serum and liver concentrations and on the sporadic occurrence of enzootic ataxia [swayback: progressive incoordination of the hind limbs, disruption of neuron and myelin development in the central nervous system; due to a deficiency of metabolizable copper], copper supplementation is recommended for grazing sheep and goats during the dry and the rainy seasons.

Considering that serum and hepatic concentrations of iron and molybdenum are within normal ranges or are marginal, it is suggested that the low copper concentrations are not related with high iron or molybdenum ingestion.

Marques, A. V. D., Soares, P. C., Riet-Correa, F., da Mota, I. O., Silva, T. L. D., Neto, A. V. B., Soares, F. A. P., and de Alencar, S. P., Serum and liver concentrations of copper, iron, zinc and molybdenum in sheep and goats in the state of Pernambuco, Pesquisa Veterinaria Brasileira, 2011, 31, 398-406.

Mean concentrations and the liver/serum concentration ratios are given in the Tables. The liver concentrations increase with the serum concentrations (not linearly, tending to level off at higher concentrations, as expected). Also, molybdenum is more concentrated in the liver.

Element

Goats

Sheep

Serum

Liver

Serum

Liver

Concentration

/μmolL-1

Concentration /mgkg-1

Concentration

/μmolL-1

Concentration /mgkg-1

Copper

11.37

+/- 2.57

152.46

+/- 79.58

9.85

+/- 2.71

158.45

+/- 83.05

Iron

25.06.

+/- 8.10

210.53

+/- 121.99

35.58

+/- 14.89

156.10

+/- 55.99

Molybdenum

0.28

+/- 0.11

6.53

+/- 4.13

0.31

+/- 0.16

8.10.

+/- 4.01

Zinc

11.79

+/- 7.42

132.91

+/- 55.28

11.9

+/- 6.07

126.43

+/- 51.50


Ratio liver/serum

goats

sheep

Copper

13.4

16.1

Iron

8.4

4.4

Molybdenum

23.3

26.1

Zinc

11.3

10.6



Molybdenum in agriculture: application of molybdenum to leaves of winter beans

The objective was to evaluate the performance of irrigated winter beans, in a no-tillage system, with increasing levels of side dressing nitrogen application (zero, 30, 60, 90 and 120 kg ha-1) and its interaction with leaf application of molybdenum (zero and 80 g ha-1). The common bean can fix nitrogen in symbiosis with Rhizobium, but the fixed nitrogen is not enough to meet the nitrogen requirement of the plant. Molybdenum application aims to improve symbiosis in the Rhizobium-common bean plant, given its importance in the metabolism nitrogen, thus being able to reduce the application of nitrogen fertilizer. The research was carried out on soil previously cultivated with corn culture. The levels of nitrogen proved consistent regarding the effects on some production components, and on dry mass of plants, providing better development of irrigated beans cultivated under no-tillage. The application of molybdenum in leaves did not influence the majority of evaluated parameters.

Barbosa, G. F., Arf, O., do Nascimento, M. S., Buzetti, S., and Freddi, O. D., Side dressing nitrogen and leaf molybdenum in the winter common bean plant, Acta Scientiarum-Agronomy, 2010, 32, 117-123.

Molybdenum in agriculture: application of molybdenum and lime to beans

For successful bean production in acidic soils attention is needed to supply important nutrients in the study area.The effects of Rhizobium inoculation, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris L. were investigated in a split-split plot design in a greenhouse and field experiment. R. inoculation, molybdenum and lime had effects on the leaf chlorophyll content (Chl), the photosynthesis (A), the intercellular CO2 concentration (Ci) and the transpiration rate (E) of Phaseolus vulgaris L. Application of Mo and lime at the highest rates (12 g of Mo per kg seed and 3 t lime ha-1 respectively) was superior to the control and the 6 g of Mo per kg seed and 2 t lime ha-1. The combination of these supplies at different levels resulted in significant interactions between some parameters.

Bambara, S. and Ndakidemi, P. A., Effects of Rhizobium inoculation, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris L, African Journal of Microbiology Research, 2009, 3, 791-798.


Molybdenum in Bacteria

Comparative analysis of the molybdate transport proteins in various bacteria and archaea is reviewed. Molybdate is transported by an ABC-type transporter comprising three proteins, ModA (periplasmic binding protein), ModB (membrane protein) and ModC, the ATPase. In the absence of the high-affinity molybdate transporter, molybdate is also transported by another ABC transporter which transports sulfate/thiosulfate as well as by a nonspecific anion transporter.

Self, W.T., Grunden, A. M., Hasona, A., and Shanmugam, K. T., Molybdate transport, Research in Microbiology, 2001, 152, 311-321.

Antimicrobial properties of ketimine molybdenum(VI) complexes

Dioxomolybdenum(VI) and oxovanadium(V) complexes of heterocyclic ketimines, 5-nitro-3-(indolin-2-one)hydrazinecarbothioamide, 5-nitro-3-(indolin-2- one) hydrazinecarboxamide , 6-nitro-3-(indolin-2-one) hydrazinecarbo- thioamide and 6-nitro3-(indolin-2-one) hydrazinecarboxamide were applied to pathogenic bacteria and fungi to assess their growth inhibition potency.

Garg, R., Fahmi, N., and Singh, R. V., Synthetic, spectral, and antimicrobial aspects of biologically relevant coordination compounds of dioxomolybdenum(VI) and oxovanadium(V), Russian Journal of Coordination Chemistry, 2008, 34, 198-203.


Molybdenum in animals

Molybdenum Concentrations in Animals

Source

Concentration /
ppm dry weight

Marine Animals

0.6 - 2.5

Coelenterates

0.7

Molluscs

2.0

Echinoderms

2.5

Crustacea

0.6

Insects

0.6

Fish

1.0

Mammals

<1.0

Bone

<2.6

Bowen, H. J. M., Trace Elements in Biochemistry, 1966, Academic Press, N. Y.
Molybdenum Concentrations in Animal Organs [2,3]

Animal

Brain

Kidney

Liver

Lung

Muscle

Spleen

Adult rat

0.24

1.0

1.8

0.37

0.06

0.52

Chicken

-

4.4

3.6

-

0.14

-

Seaducks Southeast Alaska [4]


<10

<10




bovine [5]



3.62




horse [5]


2.20





Concentrations in ppm Mo on dry weight basis.
[2] (a) Underwood, E. J.,Trace Elements in Human and Animal Nutrition, 1962, 2nd Ed. Academic Press, London, 100; (b) Kolomiitseva, M. G., Polonskaya, M. N. and Osipov, G. K., Mikroelem. Sel. Khoz. Med., 1968, 4, 183; (c) Schroeder, H. A., Balassa, J. J. and Tipton, I. H., J. Chronic Diseases, 1970, 23, 481.
[3] Tipton I. H. and Cook, M.J., Health Phys., 1963, 9, 103.
[4] Franson, J.C., Koehl, P.S., Derksen, D.V., Rothe, T.C., Bunck, C.M., Moore, J.F., Heavy-Metals In Seaducks And Mussels From Misty-Fjords-National-Monument In Southeast Alaska, Environmental Monitoring And Assessment, 1995, 36,149-167.
[5] Alonso, J.I.G., Camblor, M.G., Bayon, M.M., Marchante Gayon, J.M., Sanz Medel, A., Different quantification approaches for the analysis of biological and environmental samples using inductively coupled plasma mass spectrometry, Journal Of Mass Spectrometry, 1997, 32, 556-564.

Molybdenum in Pig liver and mussels

Molybdenum concentrations were:

pig liver 3.8 – 4.0 microg/g

mussel 0.60 – 0.63 microg/g

Jiang, C.Q., Wang, J. Z., and He, F., Spectrofluorimetric determination of trace amounts of molybdenum in pig liver and mussels, Analytica Chimica Acta, 2001, 439, 307-313.

Molybdenum tolerance of sheep, cows, horses and pigs

Sheep and cows, develop adverse reactions to feed containing 2-30 ppm molybdenum; horses and pigs tolerate feed with concentrations > 1000 ppm molybdenum.

Smyth, H.E., Hygienic standard for daily inhalation. Ind Hyg Q, 1956, 17,129-185.

Molybdenum deficiency and elevated xanthine and sulfite

Molybdenum deficiency may lead to amino acid intolerance, irritability, elevated urinary xanthine and sulfite, and reduced uric acid and sulfate. Condition cured by 160 microg Mo/d administered.

Aburnrad NN, Schneider AJ, Steel D, Rogers LS. Amino acid intolerance during prolonged total parenteral nutrition reversed by molybdate therapy. Am J Clin Nutr 198 ; 34:2551-2559.

Molybdenum and insulin in rats

Insulin resistance, hyperinsulinemia, hypertriglyceridemia and hypertension occur in rats fed with high fructose diet. Sodium molybdate has insulin-like effects in animal models of type I and type II diabetes. The effects of Mo on fructose- hypertensive male Wistar rats was investigated. Molybdate treatment prevented fructose- induced hyperinsulinemia and hypertension in rats

Guner, S., Tay, A., Altan, V. M., and Ozcelikay, A. T., Effect of sodium molybdate on fructose-induced hyperinsulinemia and hypertension in rats, Trace Elements and Electrolytes, 2001, 18, 39-46.
Molybdenum concentrations in clams and oysters

Source

Mo/mg/kg wet

clams hardshell

0.16+/- 0.33

clams softshell

0.31+/-0.38

oysters Eastern

0.08+/-0.24

oysters Pacific

below detection

Baseline values for elements in clams and oysters harvested from US coastal waters 1985/1986.

Capar, S.G., Yess, N.J., US Food-And-Drug-Administration Survey Of Cadmium, Lead And Other Elements In Clams And Oysters, Food Additives And Contaminants, 1996,13,553-560.
Effect of Cu on Molybdenum concentration in animal livers

Source of liver

Cu/mg/kg wet

Mo/mg/kg wet

Aborted horse fetus

3.74

1.61

Dead horse

4.35

1.69

Slaughtered cow

1.10

1.38

Control cow

17.7

1.37

Fly ash used in road construction blew over and contaminated pasture and water. The fly ash pH was ca 10 giving high bioavailabilityof Mo. Mo in forage 6 months after fly ash contamination 1.2mg Mo/kg dry weight (cf ‘normal’ in grasses in Denmark 0.1 - 0.3), Cu 5.0 mg Cu/kg.

Biological half life of Mo in cattle 24 h. Mo in fly ash 7 - 160 mg/kg . Absorption of Mo from gastrointestinal tract of ruminants 80 %, from humans and horses (?) 5 - 72%.

Ladefoged, O., Sturup, S., Copper Deficiency In Cattle, Sheep And Horses Caused By Excess Molybdenum From Fly-Ash - A Case-Report, Veterinary And Human Toxicology, 1995, 37, 63-65.

Trace elements including molybdenum in poultry eggs

Despite substantial interest in the trace element content of eggs by poultry breeders, nutritionists, and environmental scientists, available data about trace elements levels in eggs are scarce. Trace element contents in yolk and albumen of chicken, turkey, duck, goose, and pigeon eggs were analyzed to establish a baseline dataset and assess differences among trace element content in avian species. The selenium (Se), zinc (Zn), manganese (Mn), cobalt (Co), copper (Cu), molybdenum (Mo), vanadium (V), chromium (Cr), nickel (Ni), arsenic (As), cadmium (Cd), and thallium (Tl) contents in both yolk and albumen were measured by inductively coupled plasma mass spectrometry. One hundred twenty eggs deriving from 24 birds of each species, reared in the same poultry farm in northern Greece, were used; bird feed was common and based on cereals and legumes and contained no added vitamins or microminerals. Trace element contents in yolks were far higher than those in albumen, except for V and Ni. In yolks, the highest content for Se, Mo, and Tl were in pigeon eggs, for Zn, Mn, Cu, and Cr in turkey eggs, and for Co and Ni in goose eggs. In albumen, Se was highest in duck eggs, while Zn, Mn, and Co in pigeon ones. It is concluded that there is a substantial, up to threefold, variation for trace element contents in eggs among different domestic avian species offered the same feed.

Nisianakis, P., Giannenas, I., Gavriil, A., Kontopidis, G., and Kyriazakis, I., Variation in Trace Element Contents Among Chicken, Turkey, Duck, Goose, and Pigeon Eggs Analyzed by Inductively Coupled Plasma Mass Spectrometry (ICP-MS), Biological Trace Element Research, 2009, 128, 62-71.

Molybdenum in foodstuffs: meat

The levels of cadmium, lead, iron, zinc, selenium, manganese, copper and molybdenum in different cuts of beef, pork, lamb, chicken and foal collected from supermarkets and butcheries in Switzerland were determined by inductively coupled plasma mass spectrometry (ICP-MS) after microwave digestion. Molybdenum concentrations were in the range 0.9 and 3.2 mu g/100 g and were higher in chicken meat than in mammalian meats,

Gerber, N., Brogioli, R., Hattendorf, B., Scheeder, M. R. L., Wenk, C., and Gunther, D., Variability of selected trace elements of different meat cuts determined by ICP-MS and DRC-ICPMS, Animal, 2009, 3, 166-172.

Molybdenum in food

A useful review of the molybdenum content of foods in Germany. The molybdenum content of food (microg kg-1 dry matter) in Germany varied between 10 and 6000: 10-400 for cereal products, sugar-and starch-rich food, luxury food, bread, rolls, cake, spices and most kinds of fruits; 4000 for cucumber, herbs and vegetables and pulses are generally rich in molybdenum; animal products, are poor in molybdenum with exception of liver and kidney. Vegetable foodstuffs as part of mixed diets in Germany deliver 70% of the human intake, animal foodstuffs about 20% and beverages less than 10%

Seifert, M., Dorn, W., Muller, R., Holzinger, S., and Anke, M., The Biological and Toxicological Importance of Molybdenum in the Environment and in the Nutrition of Plants, Animals and Man Part III. Molybdenum Content of the Food, Acta Alimentaria, 2009, 38, 471-481.


Molybdenum and food

Bioaccessibility of essential elements from food

Bioaccessibility of five essential micronutrients (iron, zinc, copper, manganese and molybdenum) from the Lebanese food basket including bread, different varieties of white cheese, fruit and vegetables was evaluated using the in vitro gastrointestinal digestion model.

Bioaccessibility (%)of essential elements in foods


Mn

Fe

Cu

Zn

Mo

apple

>50

<10

>50

56

>50

bread

25

10

>50

10

>50

cheese

30

>50

>50

50

>50

cucumber

>50

10

>50

10

>50

squash

>50

10

>50

10

>50

Khouzam, Rola Bou; Pohl, Pawel; Lobinski, Ryszard, Bioaccessibility of essential elements from white cheese, bread, fruit and vegetables TALANTA, 2011,86, 425-428