Handbook of Plant Nutrition - chapter 21 doc

grown in a fluvo-aquic soil and an Oxisol, an increase in shoot vanadium concentration occurred when concentrations of more than 30 mg V kg⫺1were added to the fluvo-aquic soil, but no incr

21 Vanadium

David J Pilbeam and Khaled Drihem

University of Leeds, Leeds, United Kingdom

CONTENTS

21.1 Historical 585

21.2 Growth Effects 586

21.2.1 Growth Stimulation .586

21.2.2 Toxicity 587

21.3 Metabolism 588

21.4 Vanadium in Plant Species 589

Acknowledgment 594

References 594

21.1 HISTORICAL

The transition element vanadium exists mostly in the ⫹3, ⫹4, and ⫹5 oxidation states (Table 21.1),

with the ⫹4 and ⫹5 states predominating under oxidizing conditions in the normal soil acidity of

below pH 8 (1,2) Vanadium, with many other heavy metals, is released by anthropogenic activity, and its concentration has been steadily increasing in the environment A study on peat dating back 12,370 years from a bog in Switzerland indicated a large increase in inputs of vanadium since the industrial revolution (3) Analysis of herbarium specimens of 24 species of vascular plants and 3 bryophytes collected over many years in Spain has shown a large increase in leaf vanadium con-centrations, particularly since the 1960s (4)

In soils, the main source of vanadium is from the burning of coal, and the subsequent addition

of fly ash and bottom ash In 1988, this ash contributed 11 to 67 ⫻ 106kg V yr⫺1to soils, 25% of the total vanadium deposited (5) Agricultural and food wastes contributed 3 to 22⫻ 106kg yr⫺1, and atmospheric fallout added 3.2 to 21⫻ 106kg yr⫺1

585

TABLE 21.1 Oxidation States of Some Important Species of Vanadium

Pervanadyl VO 3 ⫹ ; V(OH)4⫹ ⫹5

Total atmospheric fallout in a typical year in recent times (1983) resulted mainly from the burn-ing of oil in electricity generation (estimated to be 6960 to 52,200⫻ 103kg ) and from industrial and domestic combustion of oil (30,150 to 141,860⫻ 103kg ) (5) Of the 15 heavy metals consid-ered in that study, vanadium was the highest to be emitted during oil combustion (5), and its pres-ence is often taken as an indicator of oil pollution (4)

In a study of microelements in the needles of white fir (Abies alba Mill.) in the Carpathian

mountains of Eastern Europe, vanadium was found in high concentrations in the vicinity of ferrous metal plants (6), and it is emitted into the atmosphere during the production of copper, nickel, iron, and steel, and during the incineration of sewage sludge (5) With the discontinuation of sewage sludge incineration in many countries, it might be expected that direct addition of vanadium to soils

in sewage sludge could increase worldwide

The natural vanadium, occurring at approximately 110 to 150 mg kg⫺1(1,7) in the crust of the Earth, is found particularly in roscoelite (KV3Si3O10(OH)2), vanadinite (Pb5(VO4)3Cl), and patronite (VS4) (1) During weathering of these rocks, vanadium is oxidized to the vanadate ion, which because

of its solubility in water across a range of pH values makes vanadium readily available to plants However, in practice, vanadium is not very mobile in soil, and in a study on a loamy sand, only a very small proportion of vanadium added to the top 7.5 cm of soil migrated down within 18 or 30 months; 81% remained in the top of the soil where it was added (2) The amount of vanadium that was removed

by HCl–H2SO4extraction of the top 7.5 cm of soil decreased by 81% during 18 months; hence, vana-dium must have been transformed to an immobile form with time Vanavana-dium is known to adsorb to iron and aluminum oxides in the clay fraction (2) Some vanadium may be precipitated as Fe(VO3)2, and some may be immobilized by anion exchange (2)

The correlation is good between soil organic matter content and the oxidizable (immobile) frac-tion of vanadium (8) Insoluble humic acid is known to reduce mobile metavanadate (VO3⫺) anions

to vanadyl (VO2⫹) cations, which probably bind to the humic acid by cation exchange (1) In an industrial area of Poland, most of the vanadium was bound to soil organic matter in a recent study

of a soil that was rich in the element The next largest fraction was the residual fraction followed,

in order, by a fraction bound to iron-manganese oxides, a fraction in exchangeable form, and finally

a fraction bound to carbonates in amounts too small to measure The much lower amounts of vana-dium in soil from an agricultural area occurred in the order of exchangeable fraction, residual frac-tion, the fraction bound to iron-manganese oxides, and the fraction bound to organic matter, with the fraction bound to carbonates being again too small to measure (9)

Uptake and accumulation are influenced by soil type, as soil composition affects the

availabil-ity of vanadium Vanadium generally is accumulated in plants in very small amounts in comparison

to the total vanadium content of the soil (1) In a comparison of soybeans (Glycine max Merr.)

grown in a fluvo-aquic soil and an Oxisol, an increase in shoot vanadium concentration occurred

when concentrations of more than 30 mg V kg⫺1were added to the fluvo-aquic soil, but no increase

occurred at concentrations of up to 75 mg V kg⫺1added to the Oxisol (10) Plant growth was inhib-ited when the concentration of vanadium supplied exceeded 30 mg kg⫺1in the fluvo-aquic soil but

was not inhibited in the Oxisol In a study on bush bean (Phaseolus vulgaris L.), the accumulation

of vanadium from a loamy sand was more than double the accumulation of cadmium and more than

300 times the accumulation of thallium (2) Concentrations of vanadium in plants are typically 0.27

to 4.2 mg kg⫺1dry weight (11) At low rates of supply, vanadium appears to stimulate plant growth, but at higher rates of supply it appears to be toxic to many plants (7)

21.2 GROWTH EFFECTS

21.2.1 G ROWTH S TIMULATION

Vanadium was considered to be a micronutrient for the green alga Scenedesmus obliquus Kützing

during experiments in which impure iron salts were being used to assess the iron requirement of the

species (12) It was difficult to confirm a similar requirement in higher plants (13) First, it is

difficult to eliminate vanadium entirely from nutrient cultures (13) Also, although vanadate is a

well-known inhibitor of plasma membrane proton-pumping ATPases, trace concentrations have been reported to benefit plant growth In an experiment on sand-grown corn (Zea mays L.), a

sup-ply of vanadium increased grain yield, probably because leaf area was increased but also possibly due to physiological effects (14) Supply of vanadium to tomato (Lycopersicon esculentum Mill.) at

0.25 mg L⫺1of nutrient solution gave greater plant height, more leaves, more flowers, and greater

plant mass than supplying no vanadium (15)

Hewitt, working with data from Welch and Huffman (16), calculated that the concentrations of

vanadium in tomato plant cells are less than 1% of the concentration of vanadium in

vanadium-deficient Chlorella cells, suggesting that vanadium is not an essential element for the growth

of higher plants (13) In the paper on which Hewitt’s calculations were based, lettuce (Lactuca

sativa L.) and tomato plants were grown to maturity in nutrient solutions containing less than

0.04 mg V L⫺1and with tissue concentrations of ⬍2 to 18 mg V kg⫺1dry weight (16) Plant growth

in this low concentration of vanadium was comparable to that in nutrient solutions containing 50 mg

V L⫺1, with tissue concentrations of 117 to 419 mg kg⫺1dry weight, whereas it might have been expected that the low concentration of vanadium should have had a beneficial effect on growth

However, iron was supplied as the citrate salt, and in work on Chlorella pyrenoidosa, vanadium

stimulated growth when iron was supplied as FeCl3but had only negligible effect when iron was

supplied as citrate or iron EDTA (17) Therefore, part of its requirement as an essential element in algae, at least, is as a replacement for unavailable iron, and supply of iron in a readily available form removes this requirement If vanadium is a beneficial element for higher plants it may be so only

when iron or other metals are limiting

21.2.2 T OXICITY

If some doubt exists about the role of vanadium as a beneficial element, there is no doubt that at

high rates of supply (10 to 20 mg L⫺1) it is harmful to plants (12) Sorghum (Sorghum bicolor

Moench.) seedlings supplied with vanadium as ammonium metavanadate at 1, 10, or 100 mg L⫺1in nutrient solutions showed no toxic effects in the 1 mg L⫺1solution, but showed a noticeable red-dening of the lower stems, and later the leaf tips, in the 10 mg L⫺1 or higher solution (7) In an experiment on bush beans planted 15 months after application of 5.6 kg VOSO4H2O ha⫺1on the surface and harvested 3 months later, growth of shoots and roots was significantly less than in

unfer-tilized plants (2)

In the experiments in which soybeans were grown in a fluvo-aquic soil or in an Oxisol, plant

growth was inhibited when the concentration of vanadium supplied exceeded 30 mg kg⫺1in the

fluvo-aquic soil, a rate of supply that gave a shoot concentration of approximately 1 mg V kg⫺1 dry matter (10) With a supply of 75 mg V kg⫺1soil, the shoot concentration was approximately

4 mg kg⫺1dry matter, and plant growth was even more depressed than with the lower supply of vanadium (10)

One of the reasons for the harmful effects of vanadium is that it induces iron deficiency

Noticeably decreased concentrations of iron were measured in leaves of a manganese-sensitive bush

bean cultivar supplied with vanadate (18) Cereals, strawberries (Fragaria X ananassa Duchesne),

and flax (Linum usitatissimum L.) are noted as being very sensitive species (19) Wheat (Triticum

aestivum L.) and barley (Hordeum vulgare L.) are more sensitive than rice (Oryza sativa L.) or

soy-bean (20) In addition to causing chlorosis from iron deficiency, vanadium has been shown to lower

the concentration of iron in roots of soybeans (21) and to lower root concentrations of magnesium and potassium in soybean (22,23) and lettuce (23) Vanadium also decreased root and hypocotyl

accumulation of molybdenum in white mustard (Sinapis alba L.) (25) and decreased calcium

con-centrations in leaves of soybean (23,24) Root and hypocotyl concon-centrations of manganese, copper,

and nickel were increased in Sinapis alba (25), and leaf concentration of manganese was increased

to toxic levels in bush bean (18) Some evidence indicates that vanadium may increase aluminum concentrations in soybeans (22)

In a field experiment with soybean, seed yields decreased with an increase in vanadium

con-centration in the soil, or more precisely with an increase in the V:(V⫹P) ratio (26) Seed yield

decreased by approximately 20% as the resin-extractable V:(V⫹P) ratio increased to 0.15 mol

mol⫺1(26), although a decrease also occurred in relation to vanadium alone (27) The negative rela-tionship between vanadium and phosphorus is not surprising given that the inhibition of ATPases

by vanadate is brought about by competitive inhibition of phosphate-binding on the enzymes

If the harmful effects of vanadium become more important with time as anthropogenic sources

increase, it would be helpful to be able to alleviate them The effects of vanadium in the soil can be

reduced by adding a chelating agent, such as γ-irradiated chitosan, to the soil (20) Furthermore, it might be expected that since vanadium induces iron deficiency in plants, increased iron supply

might alleviate vanadium toxicity, and this effect has been shown to be the case (28)

21.3 METABOLISM

Vanadium has been shown to enhance chlorophyll formation and iron metabolism of tomato plants and to enhance the Hill reaction of isolated chloroplasts (15) Corn plants that had higher grain yield

with a supply of vanadium in sand culture had increased concentrations of chlorophyll a and chloro-phyll b (14) Supply of vanadium increased the synthesis of chlorochloro-phyll through enhanced synthesis

of the porphyrin precursor δ-aminolevulinic acid in the green alga Chlorella pyrenoidosa Chick (29),

although the pH optimum for the enhancement of chlorophyll synthesis by vanadium was slightly

different from the pH optimum for enhancement of algal cell growth (30) The substitution of

vana-dium for iron in green algae highlights the involvement of both ions in chlorophyll synthesis

No clear evidence is available for the role of vanadium in chlorophyll synthesis in higher plants, but iron deficiency gives rise to lower amounts of chlorophyll per chloroplast (31), and the

require-ment for iron in chlorophyll synthesis has been narrowed down to a specific step (32) rather than to

secondary effects The requirement for iron is clear, and vanadium may possibly influence

chloro-phyll synthesis only through an effect on iron metabolism At one stage it was proposed that green

algae may have a pathway of synthesis of δ-aminolevulinic acid that is vanadium-dependent but

differs from the pathway in higher plants (13); however, such a pathway has not been identified In

recent years, genes coding for the enzymes involved in this synthesis have been identified in higher

plants and in algae, so differences in the pathway, if they exist, appear to be at the level of control

rather than in the pathway itself It is possible that vanadium is an essential cofactor for one of the enzymes of chlorophyll biosynthesis in green algae, but in higher plants this role is normally taken

on by another metal for which vanadium can substitute

Vanadate (but not vanadyl) promoted the evolution of oxygen from intact cells of Chlorella

fusca at the same concentrations that gave maximum promotion of algal growth (1 to 2µM) (33) Vanadium was thought to work in the chain of electron transport between photosystems

2 and 1 by virtue of the ability of the vanadium to change reversibly between its tetravalent and pentavalent states (33) Vanadium also increased photosystem 1 activity (but not photosystem

2 activity) in isolated chloroplasts of spinach (Spinacia oleracea L.), with an optimum at

approx-imately 20µM V (33)

Corn plants that showed enhanced grain yield with supply of vanadium had more nitrogen, phosphorus, potassium, calcium, and magnesium in the leaves, although high concentrations of vanadium decreased the concentrations of these elements (14) Vanadium was shown to increase foliar concentrations of calcium and iron in lettuce, although in these plants, yield was actually depressed by the vanadium supplied (23)

The presence of vanadium certainly affects the metabolism of plants Addition of vanadium at

1mg L⫺1to solution reduced nicotine concentrations in tobacco (Nicotiana tabacum L.) by 25%

(34) In lupin (Lupinus polyphyllus Lindl.), a negative correlation between alkaloid and vanadium

concentrations in the leaves has been observed (35)

Given the inhibitory effects of vanadate on plasma membrane ATPases, it is not surprising that

vanadium should affect metabolism Changes in concentrations of other ions in plants supplied with

vanadium could in part be due to the effects on proton-pumping APTases, although uptake of

phos-phate into isolated corn root tips was inhibited less than the activity of ATPase in the tips at the same amount of sodium vanadate supplied (36) Nevertheless, heavy exposure of these enzymes to vana-dium might be expected to stop plant transport completely Some evidence indicates that vanavana-dium may also inhibit the absorption of water (37)

Absorption of vanadium appears to be a passive process as it is a linear function of external vana-dium concentration and is not affected by putting excised roots into anaerobic conditions (38)

Absorption is highly pH-dependent, being fastest at pH 4 and dropping to a very slow rate by pH 10, although being relatively constant between pH 5 and 8 (38) This effect of pH on absorption appears

to be due to the ionic form in which vanadium is present, with VO2⫹predominating at pH 4, HVO3 predominating between pH 4 and 5, VO3⫺ predominating between pH 5 and 8, and HVO4⫺ pre-dominating at pH 9 to 10 (38) The VO2⫹form that predominates in acid soil is taken up by plants far more readily than the other forms that predominate in neutral and alkaline soils (11)

Absorption of vanadium appears to occur at the expense of calcium uptake, there being a linear decrease in calcium accumulation into sorghum cultivars with log concentration of vanadate sup-plied (39) This result is probably due to an effect on calcium channels that more than compensates

for the inhibition by vanadate of the H⫹-translocating ATPase responsible for calcium flux The

presence of calcium is required for absorption of vanadium, and this effect, together with the fact

that vanadium concentrates in the roots at up to twice the concentration in the external medium, indicates that the passive absorption cannot be purely by diffusion A concentration gradient from

outside to inside the root could be maintained by the vanadium changing form inside the root, with

up to 10% of VO3⫺taken up being reduced to VO2⫹(40), or it could be chelated (38)

Indeed, various complexes of vanadium have been detected in plants At low rates of vanadium supply, plants form low-molecular-weight complexes thought to be vanadyl amino compounds, and

at high rates of supply, plants form high molecular weight complexes, probably vanadyl cellulose compounds (41) It seems that following absorption, vanadium is partially immobilized on the root cell walls It then develops soluble complexes outside the plasmalemma and finally is absorbed into

the vacuoles within the cells (41) Concentrations in roots are usually higher than in leaves Calcium seems to accumulate in roots along with vanadium In soybeans supplied with vana-dium, both elements were concentrated in the roots, and very high concentrations of calcium have been detected in the roots of vanadium-accumulating species Perhaps, calcium may work to detoxify the vanadium (7,24) It is possible that the vanadium occurs as insoluble calcium vana-date (1) This action may be only a partially successful detoxification as it has been suggested that

the accumulation of calcium might give rise to the imbalance in other cations associated with vana-dium toxicity (24)

There does not appear to be much inhibition of absorption of vanadium by molybdate, borate,

chloride, selenate, chromate, or nitrate (38) However, in Sinapis alba nickel, manganese, and

cop-per inhibited the accumulation of vanadium in roots and hypocotyls, whereas molybdate decreased its accumulation in the hypocotyls and enhanced its accumulation in the roots (25)

21.4 VANADIUM IN PLANT SPECIES

In general, lower plants contain more vanadium than seed-bearing plants, and older parts contain more than younger parts (7) Despite this overall trend, some angiosperms seem to be accumulator plants (Table 21.2) In an experiment where sorghum seedlings showed noticeable harmful effects

TABLE 21.2

A List of Concentrations of Vanadium in Various Plant Species

Plant Type of Concentration in Dry Plant Species Part Culture Matter (mg kg⫺⫺1 ) Reference Comments

Allium macropetalum Root Wild 133 7 Accumulator species Rydb (onion)

Anethum graveolens Shoot Field 0.84 44

L (dill)

Astragalus conferti florus Shoot Wild 144 7 Accumulator species Gray (yellow milkvetch)

Astragalus preussi Shoot Wild 67 7 Accumulator species

A Gray (milkvetch)

Avena sativa L (oat) Seed Nutrient 0.055 45 No added V

Brassica napus L Seed Nutrient 0.018 45 No added V

Brassica oleracea var Florets Field 1.09 ⫻ 10 ⫺3 44

botrytis L (cauliflower)

Carthamus tinctorius L. Seed Nutrient 0.019–0.021 45 No added V

Castilleja angustifolia Shoot Wild 22 7 Accumulator species

G Don

(desert paintbrush)

Chrysothamnus Shoot Wild 37 7 Accumulator species

viscidi florus Nutt

(rabbitbrush)

Conifers (unidenti fied Leaves Soil 0.69 7

species)

Cowania mexicana Shoot Wild 7.4 7 Accumulator species D.Don var.

stansburiana

(cli ff rose)

Cucumis sativus L. Fruit Field or 5.6 ⫻ 10 ⫺2 44

(unidenti fied species)

(unidenti fied species)

Equisetum sp Soil 2.4 7

(horsetail)

Eriogonum in flatum Shoot Wild 15 7 Accumulator species Torr & Frém.

(desert trumpet)

Ferns (unidentified Fronds Soil 1.28 7

species)

Forbs (unidenti fied Leaves Soil 1.20 7

species excluding

legumes)

Fragaria X ananassa Fruit Field 3.1 ⫻ 10 ⫺2 44

Duchesne (strawberry)

Fragaria vesca L Fruit Wild 4.1 ⫻ 10 ⫺2 44

(wild strawberry)

Continued

TABLE 21.2 (Continued )

Plant Type of Concentration in Dry Plant Species Part Culture Matter (mg kg⫺⫺1 ) Reference Comments

Glycine max Merr Shoot Nutrient 2.3 28 No V, no Fe, then

high Fe ⫹ V

low Fe ⫹ V

high Fe ⫹ V

Pods Soil in 27/29 24 Control/plus extra

(Control is no metals added)

(Control is no metals added)

(Control is no metals added)

metals (including V) (Control is no metals added)

Upper Nutrient 0/0 24 3.0/6.0 mg V L⫺1 leaves solution

leaves

fluvo-aquic soil

fluvo-aquic soil

Youngest Vermiculite 53.6 21 104-day-old plants,

Oldest solution 45.6 104-day-old plants,

100µmol V L ⫺1

no added V

(unidenti fied species)

Continued

TABLE 21.2 (Continued )

Plant Type of Concentration in Dry Plant Species Part Culture Matter (mg kg⫺⫺1 ) Reference Comments

Gutierezzia divaricata Shoots Soil 9.3 7 Accumulator species (snakeweed)

Hordeum vulgare L Seeds Nutrient 0.028 45 No added V

Lactuca sativa L Shoots Field 0.58 44

Larrea tridentata Leaf Wild 1.8–3.4 46 Plants in geothermal

(unidenti fied species)

(unidenti fied species)

Linum usitatissimum Seed Nutrient 0.018 45 No added V

Lycopersicon Fruit Field or 0.53 ⫻ 0 ⫺3 44

esculentum Mill glasshouse

solution

Fruit Rock-wool 0.126 ⫻ 10 ⫺3 47 Normal EC

and nutrient (fresh mass)

(fresh mass) Fruit Soil and nutrient 0.124 ⫻ 10 ⫺3 Normal EC

solution (fresh mass)

Malus pumila Mill Fruit Field 0.86 ⫻ 0 ⫺2 44

[M domestica

Borkh.] (apple)

Medicago sativa Shoots Field 0.115 48

L (alfalfa)

species)

Oryza sativa L (rice) Shoots Nutrient solution 530 20 10 mg V L⫺1

Oryzopsis hymenoides Shoot Soil 10 7 Accumulator species Ricker (ricegrass)

Petroselinum crispum Shoots Field 4.52 44

Nyman ex A.W Hill

(parsley)

Continued

TABLE 21.2 (Continued )

Plant Type of Concentration in Dry Plant Species Part Culture Matter (mg kg⫺⫺1 ) Reference Comments

Phaseolus vulgaris L Primary Nutrient 2.6 18 0.05 mg V L⫺1

leaf

leaf

Mn-tolerant cultivar Primary leaf 4.7 0.05 mg V L⫺1

leaf

leaf

Pisum sativum L (pea) Shoot Nutrient 15.0 28 No V, no Fe, then

high Fe ⫹ V

low Fe ⫹ V

high Fe ⫹ V

Plantago insularis Leaf Wild 1.9–3.2 46 Plants in geothermal

plantain)

Raphanus sativus L. Roots Field 1.26 44

(radish)

Solanum tuberosum L Tuber Field 0.64 ⫻ 10 ⫺2 44

(potato)

Continued

TABLE 21.2 (Continued )

Plant Type of Concentration in Dry Plant Species Part Culture Matter (mg kg⫺⫺1 ) Reference Comments

Triticum aestivum L Seed Nutrient 0.046 45 No added V

Zea mays L (corn) Leaves Field 0.244 48

when grown in 10 mg V L⫺1in the nutrient solution, the selenium-accumulator Astragalus preussi

A Gray was not affected by 100 mg V L⫺1and accumulated vanadium in the tissues (7)

Chicory (Cichorium intybus L.) and dogfennel (Eupatorium capillifolium Small) have been

suggested to have potential as indicators of vanadium bioavailability (42) Since 1981, the Bavarian State Office for Environmental Protection has been analyzing samples of the moss Hypnum

cupres-siforme L as indicators of emission-derived metals, including vanadium (43).

Even in crop species that are sensitive to vanadium, there are genotypes that are less affected by

the element In a study in which soybean was found to be sensitive to the V:(V⫹P) ratio, one cultivar

showed very little sensitivity to either element (27) Although concentrations of 10 to 20 mg V L⫺1 vanadium in nutrient solutions are generally regarded as harmful to plants, some bush bean and lettuce genotypes have been affected adversely by concentrations as low as 0.20 mg V L⫺1(18,23)

ACKNOWLEDGMENT

We thank Dr P A Millner for stimulating conversation on the role of vanadium in plant biochemistry

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