Micronutrients in Crop Production

Micronutrients in Crop Production

MICRONUTRIENTS IN CROP PRODUCTION N. K. Fageria,1 V. C. Baligar,2 and R. B. Clark3 1 National Rice and Bean Research Center of EMBRAPA ˆ Santo Antoni...

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MICRONUTRIENTS IN CROP PRODUCTION N. K. Fageria,1 V. C. Baligar,2 and R. B. Clark3 1

National Rice and Bean Research Center of EMBRAPA ˆ Santo Antonio de Goi´as-GO, 75375-000, Brazil 2 Alternate Crops and Systems Research Laboratory Beltsville Agricultural Research Center, USDA-ARS Beltsville, Maryland 20705 3 Appalachian Farming Systems Research Center, USDA-ARS Beaver, West Virginia 25813

I. Introduction II. Status in World Soils III. Soil Factors Affecting Availability A. pH B. Organic Matter C. Temperature, Moisture, and Light IV. Factors Associated with Supply and Acquisition A. Deficiencies and Toxicities B. Supply and Uptake C. Oxidation and Reduction D. Rhizosphere E. Interactions with Other Elements V. Improving Supply and Acquisition A. Soil Improvement B. Soil and Foliar Fertilization C. Plant Improvement D. Microbial Associations E. Improved Disease and Insect Resistance and Tolerance VI. Conclusion References

The essential micronutrients for field crops are B, Cu, Fe, Mn, Mo, and Zn. Other mineral nutrients at low concentrations considered essential to growth of some plants are Ni and Co. The incidence of micronutrient deficiencies in crops has increased markedly in recent years due to intensive cropping, loss of top soil by erosion, losses of micronutrients through leaching, liming of acid soils, decreased proportions of farmyard manure compared to chemical fertilizers, increased purity of chemical fertilizers, and use of marginal lands for crop production. Micronutrient deficiency problems are also aggravated by the high demand of modern crop cultivars. Increases in crop yields from application of micronutrients have been reported in many parts of the world. Factors such as pH, redox potential, biological 185 Advances in Agronomy, Volume 77 Copyright 2002, Elsevier Science (USA). All rights reserved. 0065-2113/02 $35.00

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FAGERIA et al. activity, SOM, cation-exchange capacity, and clay contents are important in determining the availability of micronutrients in soils. Plant factors such as root and root hair morphology (length, density, surface area), root-induced changes (secretion of H+, OH−, HCO3−), root exudation of organic acids (citric, malic, tartaric, oxalic, phenolic), sugars, and nonproteinogenic amino acids (phytosiderophores), secretion of enzymes (phosphatases), plant demand, plant species/cultivars, and microbial associations (enhanced CO2 production, rhizobia, mycorrhizae, rhizobacteria) have profound influences on plant ability to absorb and utilize micronutrients from soil. The objectives of this article are to report advances in research on the micronutrient availability and requirements for crops, in correcting deficiencies and toxicities in soils and plants, and in increasing the ability of plants to acquire needed amounts  C 2002 Elsevier Science (USA). of micronutrient elements.

I. INTRODUCTION Essential nutrients may be defined as those without which plants cannot complete their life cycle, irreplaceable by other elements, and directly involved in plant metabolism. Based on the quantity required, nutrients are divided into macro- and micronutrients. Macronutrients are required in large quantities by plants compared to micronutrients. Micronutrients have also been called minor or trace elements, indicating that their concentrations in plant tissues are minor or in trace amounts relative to the macronutrients (Mortvedt, 2000 ). The essential micronutrients for field crops are B, Cu, Fe, Mn, Mo, and Zn. The accumulation of these micronutrients by plants generally follows the order of Mn > Fe > Zn > B > Cu > Mo. This order may change among plant species and growth conditions (e.g., flooded rice). Other mineral nutrients at low concentrations considered essential to the growth of some plants are Ni and Co. Convincing evidence exists to indicate that Ni is essential for certain plants (Brown et al., 1987; Eskew et al., 1983). Even though Co stimulates growth of certain plants, it is not considered essential according to the Arnon and Stout (1939) definition of essentiality. Cobalt is essential for the fixation of N2 by bacteria, but is not required by higher plants (Ahmed and Evans, 1960; Marschner, 1995; Needham, 1983). Rhizobia and other N2-fixing microorganisms have absolute Co requirements whether growing inside or outside root nodules regardless of N source (N2 fixation or mineral N) (Marschner, 1995). Even so, Co is essential for animal nutrition as a component of vitamin B12 (Needham, 1983). Chlorine and Si have often been referred to as micronutrients, even though their concentrations in plant tissue are often equivalent to those of macronutrients. Chlorine will be considered in this article, but since recent reviews have appeared about Si (Epstein, 1994, 1999; Savant et al.,1997, 1999), this element will not be

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considered. Possibly, other essential micronutrients will be discovered in the future because of the recent advances in solution culture techniques and the availability of highly sensitive analytical instruments. Based on physicochemical properties, the essential plant micronutrients are metals except for B and Cl. Even though micronutrients are required in small quantities by field crops, their influence is as important as the macronutrients in crop production. Except for B and Cl, the micronutrients are commonly constituents of prosthetic groups that catalyze redox processes by electron transfer such as with the primary transition elements Fe and Mn and to some extent Cu and Mo. Micronutrients normally form enzyme–substrate complexes (Fe and Zn) and/or enhance enzyme reactions by influencing molecular configurations between enzymes and substrates (Zn) (R¨omheld and Marschner, 1991). Micronutrient deficiencies in crop plants are widespread because of (i) increased micronutrient demands from intensive cropping practices and adaptation of high yielding cultivars which may have higher micronutrient demand, (ii) enhanced production of crops on marginal soils that contain low levels of essential nutrients, (iii) increased use of high analysis fertilizers with low amounts of micronutrient contamination, (iv) decreased use of animal manures, composts, and crop residues; (v) use of soils that are inherently low in micronutrient reserves, and (vi) involvement of natural and anthropogenic factors that limit adequate plant availability and create element imbalances. Plant acquisition of micronutrients is affected by numerous soil, plant, microbial, and environmental factors. Parent material, minerals containing micronutrients, and soil formation processes influence micronutrient availability to plants. Solid-phase materials are important in determining solubility relationships of nutrients in soils (Lindsay, 1991). Available micronutrients in soil are derived from weathering of underlying parent materials, natural processes (e.g., gases from volcanic eruption, rain/snow, marine aerosols, continental dust, forest fires), and anthropogenic processes (industrial and automobile discharges, addition of fertilizers, lime, pesticides, manures, sewage sludges). Soil micronutrients exist in solid phases like primary minerals, secondary precipitates, and adsorbed on clay surfaces (Lindsay, 1991; Shuman, 1991). Soil adsorption reactions are important in determining the bioavailability of B, Cu, Mo, and Zn. Micronutrients in solid phases are not immediately available to plants. Only about 10% of micronutrients in soil are soluble and/or in exchangeable forms for plant acquisition (Lake et al., 1984). Fluctuating temperatures, moisture, and anthropogenic factors change micronutrient concentrations, forms, and distribution among various phases in soil. Soil pH, redox potential, and soil organic matter (SOM) profoundly affect the bioavailability of micronutrients (Stevenson, 1986; Tate, 1987). For most soils, soil SOM contains the largest pool of labile micronutrients in soil and influences micronutrient cycling, distribution of naturally occurring organic ligands, speciation and form (organic or inorganic) of elements in soil solution, and nature

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and stability of micronutrient complexes with humic and fulvic acids, especially with microbe conversion of SOM (Stevenson, 1991). The importance of SOM for influencing micronutrient retention follows the sequence of Cu > Zn > Mn (McGrath et al., 1988). Most metallic micronutrients in soil are complexed by both inorganic and organic ligands. Organic ligands act as carriers to plant roots (Lindsay, 1979), and Cu, Zn, and Mn form stable complexes, especially with carboxyl and phenolic groups, to make these minerals less available to plants (Stevenson, 1991). Organic substances like humic and fulvic acids formed in SOM degradation and transformation are also important in micronutrient cycling (Stevenson, 1986). Plant factors such as root and root hair morphology (length, density, surface area), root-induced changes (secretion of H+, OH−, HCO3−), root exudation of organic acids (citric, malic, tartaric, oxalic, phenolic), sugars, and nonproteinogenic amino acids (phytosiderophores), secretion of enzymes (phosphatases), plant demand, plant species/cultivars, and microbial associations (enhanced CO2 production, rhizobia, mycorrhizae, rhizobacteria) have profound influences on plant ability to absorb and utilize micronutrients from soil (Barber, 1995; Baligar and Fageria, 1997; Marschner, 1995). Macro- and micronutrients have long been recognized as being associated with changes in plant susceptibility or tolerance and resistance to diseases and pests (Engelhard, 1990; Graham and Webb, 1991). Even though research information on the mineral nutrition of plants has advanced significantly in recent years, most of the advances have been associated with macronutrients. Reasons for this may have been that micronutrients are required in such small amounts, and their deficiencies have not been systematically verified under field conditions. The objectives of this article are to report advances in research on the micronutrient availability and requirements for crops, in correcting deficiencies and toxicities in soils and plants, and in increasing the ability of plants to acquire needed amounts of micronutrient elements.

II. STATUS IN WORLD SOILS The amounts and distribution of micronutrients in soils are influenced by parent materials, levels and form of SOM, pH, Eh (oxidizing conditions), mineralogy, particle size distribution, soil horizon, soil age, soil formation processes, drainage, vegetation, and microbial, anthropogenic, and natural processes (Baligar et al., 1998; Stevenson, 1986; Tate, 1987). Micronutrient concentrations are generally higher in surface soil horizons (Ap) and decrease with soil depth. In spite of the relatively high total concentrations of micronutrients reported in soils on a global basis, micronutrient deficiencies have been frequently reported on many crops

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grown in various parts of the world (Cakmak, Sari et al., 1996; Fageria, 2000a; Galr˜ao, 1999; Graham et al., 1992; Grewal and Graham, 1999; Mandal and Mandal, 1990; Martens and Lindsay, 1990). It has been estimated that 3.95 billion ha of the world’s ice-free land area is subject to mineral stresses for plants, with 14% of this area being subject to potential micronutrient stresses (Gettier et al., 1985). The reasons for micronutrient deficiencies are that these elements have not usually been applied regularly to soils through fertilization. Furthermore, increased crop yields, loss of micronutrients through leaching, liming of soils, decreased use of manures compared to chemical fertilizers, and increased purity of chemical fertilizers without micronutrient additions have contributed to accelerated exhaustion of available micronutrients in soils. Hidden micronutrient deficiencies may be more widespread than has generally been suspected. Potential micronutrient deficiencies/toxicities associated with major soil groups (Table I), common soil

Table I Potential Micronutrient Deficiencies or Toxicities Associated with Major Soil Groupsa Element problem Soil order Andosols (Andepts) Ultisols Ultilsols/Alfisols Spodosols (Podsols) Oxisols Histosols Entisols (Psamments) Entisols (Fluvents) Mollisols (Aqu), Inceptisols, Entisols, etc. (poorly drained) Mollisols (Borolls) Mollisols (Ustolls) Mollisols (Aridis) (Udolls) Mollisols (Rendolls) (shallow) Vertisols Aridisols Alfisols/arid Entisols Alfisols/Utisols (Albic) (poorly drained) Alfisols/Aridisols/Mollisols (Natric) (high alkali) Aridisols (high salt)

Soil group

Deficiency

Andosol Acrisol Nitosol Podsol Ferralsol Histosol Arensol Fluvisol

B, Mo Most micronutrients

Gleysol Chernozem Kastanozem Phaeozem Rendzina Vertisol Xerosol Yermosol

Mn Fe, Mn, Zn Cu, Mn, Zn Fe, Mn, Zn Fe Fe, Zn Co, Fe, Zn

Planosol

Most micronutrients

Solenetz Solonchak

Cu, Fe, Mn, Zn

Most micronutrients Mo Cu Cu, Fe, Mn, Zn

Toxicity

Fe, Mn Mn Fe, Mn

Fe, Mn Fe, Mo

Mo

B, Cl

a Modified from Baligar and Fageria (1999); Clark (1982); Dudal (1976); S. W. Buol, North Carolina State University, Raleigh; H. Eswaren, USDA-NRCS, Washington, DC.

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FAGERIA et al. Table II Major Soil Minerals Containing Micronutrientsa

Element B

Cl

Cu

Fe

Mn

Mo

Zn

Ni

Co

a

Type Borates (hydrous) Borates (anhydrous) Complex borosilicates Sylvite Kainite Langbeinite Carbonates Oxides Simple sulfides Complex sulfides Carbonates Oxides Sulfides Sulfates Carbonates Simple oxides Complex oxides Silicates Oxides Molybdates Sulfides Carbonates Sulfides Silicates Pentlandite Awaruite Cohenite Haxonite Nickel Cobaltite Skutterudite Erythrite

Mineral Borax—Na2B4O7·10H2O; Kernite—Na2B4O7·4H2O; Colemanite—Ca2B6O11·5H2O; Ulexite—NaCaB5O9·4H2O Ludwigite—Mg2FeBO5; Kotoite—Mg3(BO3)2 Tourmaline; Axinite KCl KCl; MgSO4·3H2O K2SO4·2MgSO4 Malachite—Cu2(OH)2CO3; Azurite—Cu3(OH)2(CO3)2 Cuprite—Cu2O; Tenorite—CuO Chalcocite—Cu2S; Covellite—CuS Chalcopyrite—CuFeS2; Bornite—Cu3FeS4; Digenite—Cu9S5; Enargite—Cu3AsS4; Tetrjedrote—Cu12Sb4S13 Siderite—FeCO3 Hematite—Fe2O3; Goethite—FeOOH; Magnetite—Fe3O4 Pyrite—FeS2; Pyrrhotite—Fe1–xS Jarosite—KFe3(OH)6(SO4)4 Rhodochrosite—MnCO3 Pyrolusite—MnO2; Hausmannite—Mn3O4; Manganite—MnOOH Braunite—(Mn, Si)2O3; Psilomelane—BaMg9O18·2H2O Rhodanate—MnSiO3 Ilsemanite—Mo3O8·8H2O Wulflenite—PbMoO4; Powellite—CaMoO4; Ferrimolybdite—Fe2(MoO4)·8H2O Molybdenite—MoS2 Smithsonite—ZnCO3 Sphalerite—ZnS Hemimorphite—Zn4(OH)2Si2O7·H2O (Fe, Ni)9S8 Ni3Fe (Fe,Ni)3C (Fe,Ni)23C6 Ni CoAsS CoAs2–3 Co3(AsO4)·8H2O

From Chesworth (1991), Dana and Dana (1997), Krauskopf (1972), and Mortvedt (2000)

minerals containing various micronutrient elements (Table II), and concentration ranges of micronutrients in soils and plants (Table III) have been provided to help define where micronutrient problems might occur. Concentrations of B in soils range from about 2 to 100 mg kg−1 (mean of 10 mg kg−1) and generally occurs as H3BO3/B(OH)3 (Goldberg, 1993). Soils

Table III

<10 <2000 3–5

<50 10–20 <0.1 15–20 1.0–5 <0.2

H3BO3; BO3−; B4O72− Cl− Cu2+

Fe2+; Fe3+ Mn2+ MoO42− Zn2+ Ni2+ Co2+

B Cl Cu

Fe Mn Mo Zn Ni Co

50–250 20–300 0.1–0.5 20–100 0.1–5 0.2–0.5

10–100 2000–20000 5–20

Sufficient

>1000 300–500 10–50 100–400 10–100 15–50

50–200 >20000 20–100

Toxic

b

Bennett (1993) and McBride (1995). Alloway (1995a) (critical level above which toxicity is likely). c Kabata-Pendias and Pendias (1992). d Marschner (1995).

a

Critical

Form absorbed

Element

Concentration range in plantsa (mg kg−1)

200–500,000 7–10,000 0.1–40 1–900 0.4–1000 0.1–70

2–150 20–900 2–250

Normal

1000–3000 2–13 70–400 100 25–50

15–25 70–200 60–125

Critical total

Concentration in soilb,c (mg kg−1)

K. Warington(1923) T. C. Broyer et al. (1954) A. L. Sommers, C. B. Lipman, and G. MacKinney (1931) J. Sachs (1860) Knop. J. S. McHargue (1922) D. I. Arnon and P. R. Stout (1939) A. L. Sommers and C. B. Lipman (1926) P. H. Brown et al. (1987)

Demonstration of essentialityd

Essential Micronutrients for Plant Growth, Principal Forms Absorbed, Concentration Ranges in Plants and Soils, and Persons Demonstrating Essentiality in Plants

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FAGERIA et al.

formed from igneous rock contain less B than soils formed from marine sediments. Soils derived from granite, igneous, and acidic rocks and metamorphic sediments are often poor in B (Gupta, 1979). Low B soils are usually strongly weathered (Acrisols, Podzols, Ferralsols), coarse textured (Arenosols), and shallow (Lithosols) (Shorrocks, 1997). In acidic rocks and metamorphic sediments, B occurs in tourmaline minerals and is not readily available to plants. Boron adsorption usually increases with increasing soil solution pH, temperature, ionic strength, and nature of adsorbed cations (Goldberg, 1993, 1997). The amount of B adsorbed in fine-textured soils usually increases with enhanced clay contents. For example, montmorillonitic clays normally adsorb greater amounts of B than illitic clays (Goldberg and Glaubig, 1986). Competitive anion effects on B adsorption increased in the order of P > Mo > S even though the competitive effect was low, indicating that B adsorption sites are generally specific for B (Goldberg, 1997; Goldberg, Forster, and Lesch et al., 1996). The B-adsorbing surfaces in soils are commonly Al and Fe oxides, Mg hydroxides, clay minerals, Ca carbonates, and organic matter (OM). The distribution of B between soil solution and adsorption surfaces is affected by clay mineral types, content, and specific surface areas, mineralogy of sand/silt fractions, sesquioxides, SOM content, pH, ions on exchange sites, and salinity (Elrashidi and O’Conner, 1982; Evans and Sparks, 1983; Gupta et al., 1985). These soil factors also affect the retention of B in soils (Gupta, 1993). The availability of B is commonly reduced in soils high in Al oxides (Bingham et al., 1971) as well as in volcanic ash soils (Sillanp¨aa¨ and Vlek, 1985). In soil, B is normally present as nonionized molecules and easily lost by leaching. In arid and semiarid regions particularly, B toxicity can be of major concern (Gupta, 1979). Chlorine is ubiquitous in soils and occurs in aqueous solutions such as Cl−. Soil Cl is not tightly held by soil-exchange sites and is readily leached. Chlorine is commonly added to soil with manures and fertilizers(KCl), rainfall, sea spray, and irrigation waters (Needham, 1983). Copper is mostly found in silt and clay fractions of soil and usually present in carbonate fractions in alkaline soils and in Fe oxide fractions in acid soils (Shuman, 1991). Concentrations of Cu in soils range from about 2 to 100 mg kg−1 (mean of 30 mg kg−1) (Mortvedt, 2000). Crops grown in soils developed from sand, sandstones, acid igneous rocks, and calcareous materials often exhibit Cu deficiency, but deficiencies are not generally found on plants grown in clays and in soils formed from basic rocks (Jarvis, 1981a). In the United States, soils formed from weathered bed rocks have high Cu, whereas soils formed in the lower Atlantic coastal plains have low Cu (Kubota, 1983). Organic, peat, and muck soils generally have low amounts of labile Cu (Oplinger and Ohlrogge, 1974). When histosols are brought under cultivation, plants commonly exhibit Cu deficiency, which has been termed as a “reclamation disease” (Welch et al., 1991). Iron is the most abundant of the micronutrients in the lithosphere (Mortvedt, 2000). Soil concentrations of Fe range from 7000 to 500,000 mg kg−1 (mean of

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38,000 mg kg−1 or 3.8% in soil) (Lindsay, 1979). Most Fe in the Earth’s crust is in the form of ferromagnesium silicate. Iron is precipitated as Fe oxides or hydroxides during weathering, and small fractions of Fe are incorporated into secondary silicate materials (Schwertmann and Taylor, 1977). Iron deficiency occurs commonly on plants grown in calcareous and noncalcareous coarse-textured soils, especially in arid/semiarid regions. However, Fe deficiency can also occur on plants grown in acid soils. About 4.8 million ha of land west of the Mississippi river in the United States (intermountain region) is prone to Fe deficiency in “Fe-inefficient” crops (Mortvedt, 1975). Alkaline, calcareous, and acidic sandy soils in Florida have also been prone to Fe deficiency on citrus (Welch et al., 1991). Iron deficiency has also been closely related to Ca carbonate equivalency and soluble salts in soil (Franzen and Richardson, 2000). High soil pH, SOM, CaCO3, HCO3−, and Ca contents have also been related to decreased Fe acquisition in some plants (K¨oseoglu, 1995). Iron deficiency also occurs in various regions of Europe, east India, Bangladesh, and in most Mediterranean and west African countries (Welch et al., 1991). Low Fe soils and Fe-deficient crops have been reported for certain areas of Malta, Turkey, Zambia, and Mexico (Sillanp¨aa¨ , 1982), Indonesia (Katyal and Vlek, 1985), several Central and South American countries (Leon et al., 1985), and in south Australia, Victoria, and western Australia (Donald and Prescott, 1975). Excess Fe (toxicity) has been reported on rice grown under flooded conditions in acid soils of China, Vietnam, Thailand, Burma, Bangladesh, Sri Lanka, Malaysia, Phillippines, and Indonesia (Vose, 1982). Kang and Osiname(1985) also reported Fe toxicity on plants grown in the acid soil belt of equatorial Africa, which includes Senegal, Gambia, Liberia, and Sierra Leone. Manganese is the 10th most abundant element in the Earth’s crust. Soil Mn concentrations range from about 20 to 3000 mg kg−1 (mean of 600 mg kg−1) (Lindsay, 1979). Soil Mn appears in primary and secondary minerals, is sorbed onto mineral and OM surfaces, and incorporated into soil organisms and in soil solution. Soils derived from crystalline shales and acid igneous rocks have low reducible Mn, and soils derived from basalt, limestone, and shale commonly have high Mn (Glinski and Thai, 1971). High extractable Mn has been reported for Inceptisols and Vertisols and low extractable Mn has been reported for Ultisols and Oxisols (Lombin, 1983). Labanouskas (1966) and Reuter et al. (1988) grouped the world soils with less than adequate levels of available Mn as (i) shallow, peaty, marsh, and alluvial soils developed from calcareous parent materials; (ii) calcareous soils with poor drainage and high OM, calcareous black sands, and calcareous grassland soils recently brought into cultivation; (iii) soils occurring over limed and reclaimed acid heath soils; and (iv) sandy acid soils containing low native Mn. Manganese deficiency has been reported for plants grown in coarse-textured and poorly drained coastal plains soils of the United States (Reuter et al., 1988) and in soils of Central America, Bolivia, and Brazil (Leon et al., 1985). In Europe, Mn deficiency has been reported for plants grown in peaty (England and Denmark),

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coarse-textured (Sweden and Denmark), coarse/fine-textured (Netherlands), and podzolic and brown forest (Scotland) soils (Welch et al., 1991). Manganese deficiency has also been reported on plants grown in semiarid regions of China, India, southeast and western Australia, Congo, Ivory Coast, Nigeria, and other western African countries. Manganese toxicity on crop plants grown in many parts of the world has been reported to be more important than Mn deficiency (Foy, 1984; Welch et al., 1991). Molybdenum is the least abundant of the micronutrients in the lithosphere (Mortvedt, 2000), and soil concentrations range from about 0.2 to 5 mg kg−1 (mean of 2 mg kg−1). Plants exhibiting Mo deficiency usually occur on plants grown in broad areas of acid well-drained soils and in soils formed from parent materials low in Mo. In Australia, Mo deficiency occurred on crops grown in soils derived from sedimentary rocks, basalts, and granites (Anderson, 1970). Peaty, alkaline, and poorly drained soils commonly have high Mo. Iron oxides adsorb more Mo than Al oxides (Jones, 1957), and Mo adsorption on clays followed the sequence of montmorillonite > illite > kaolinite (Goldberg, Forster et al., 1996). Hydrous ferric oxides or ferric oxide molybdate complexes and insoluble ferric molybdates may form in well-aerated soils so that Mo solubility and availability to plants are low (Welch et al., 1991). In poorly drained soils, formation of soluble ferrous molybdates or molybdites may lead to high Mo availability to plants. Plants grown in high Mo soils of the intermountain valleys of western United States have been reported to accumulate high Mo which has induced “molybdenosis” (Cu deficiency) in cattle (Welch et al., 1991). Zinc deficiency is a worldwide nutritional constraint for crop production. About 50% of soils used for cereal production in the world contain low levels of plantavailable Zn, which reduces not only grain yield but also nutritional grain quality (Graham and Welch, 1996). Total Zn concentrations in soils range from about 10 to 300 mg kg−1 (mean of 50 mg kg−1)(Lindsay, 1979). Zinc-deficient soils occur in both tropical and temperate regions, but are widespread in Mediterranean countries like Turkey (Cakmak et al., 1997), and in New South Wales, Queensland, and western and south Australia (Donald and Prescott, 1975; Sillanp¨aa¨ and Vlek, 1985). In China, Zn deficiency has been reported on plants grown in calcareous, desert, and paddy soils along the Yangtze river (Takkar and Walker, 1993). In Africa, Zn deficiency has been observed on plants grown in Alfisols and Ultisols (Cottenie et al., 1981) and in low Zn soils of Niger, Guinea, Ivory Coast, Sierra Leone, Sudan, and Zimbabwe, which has often been induced by lime additions to increase soil pH to near 7. In Asia, Zn deficiency is common for plants grown in arid and semiarid soils (Katyal and Vlek, 1985; Welch et al., 1991). Zinc deficiency in the United States has occurred mostly in plants grown in sandy, well-drained acid soils, and in soils formed from phosphate rock parent materials of the southeast. In the Cerrado soils of Brazil (Oxisols and Ultisols), Zn deficiency is widespread (Fageria, 2000b; Lopes and Cox, 1977).

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Serpentine (ultramafic) soils are usually high in Ni, Co, Fe, and Mg, but low in Ca. Nickel levels in soils are usually adequate to provide plant needs. No evidence of Ni deficiency for soil-grown plants has been reported (Dalton et al., 1985), but Ni toxicity has been of concern for plants grown in soils receiving industrial wastes (sewage sludges, by-products) (Marschner, 1995). Cobalt deficiency has been reported for ruminant animals grazing forages grown in soils low in Co such as New Zealand, south and western Australia, The Netherlands, and the United States (Michigan and northeastern states) (Miller et al., 1991). Cobalt is adsorbed on Mn oxides, and liming tends to reduce Co availability to plants.

III. SOIL FACTORS AFFECTING AVAILABILITY Many soil factors such as pH, SOM, temperature, and moisture affect the availability of micronutrients to crop plants. The effects of these factors vary considerably from one micronutrient to another as well as in their relative degree of effectiveness. The availability of micronutrients is largely controlled by the same soil factor(s) where good correlations exist between plant concentrations of two or more micronutrients. The relationships associated with each of the many soil factors are complicated, even though correlations between many factors can be explained with relatively high certainty. A good example of this is the highly significant negative correlation between Mo and Mn. The availability of both Mo and Mn is so strongly affected by soil pH that the other factors are of limited value. While Mn in plants decreases extensively with increasing soil pH, Mo increases, and deficiencies of both Mn and Mo are not expected or do not usually occur in the same soil. Manganese deficiency is often combined with excess Mo and vice versa (Sillanp¨aa¨ , 1982). Copper, Mn, and Zn were predominantly in organically bound forms in Spodosols of Florida, whereas these elements were organically bound and associated with Mn oxides and amorphous forms in Alfisols and Entisols (Zhang et al., 1997a). Available concentrations of Co, Cu, Ni, and Zn increased with increased amounts of clay (Lee et al., 1997).

A. pH Soil pH influences solubility, concentration in soil solution, ionic form, and mobility of micronutrients in soil, and consequently acquisition of these elements by plants (Fageria, Baligar and Edwards, 1990; Fageria, Baligar, and Jones, 1997). As a rule, the availability of B, Cu, Fe, Mn, and Zn usually decreases, and Mo increases as soil pH increases. These nutrients are usually adsorbed onto sesquioxide soil surfaces. Table IV summarizes important changes in micronutrient concentrations

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FAGERIA et al. Table IV Influence of Soil pH on Micronutrient Concentrations in Soil and Plant Uptakea

Element B Cl

Influence on concentration/uptake Increasing soil pH favors adsorption of B. This element generally becomes less available to plants. Availability and uptake of B decrease dramatically at pH > 6.0. Chloride is bound tightly by most soils in mildly acid to neutral pH soils and becomes negligible to pH 7.0. Appreciable amounts can be adsorbed with increasing soil acidity, particularly by Oxisols and Ultisols, which are dominated by kaolinitic clay. Increasing soil pH generally increases Cl uptake by plants.

Cu

Solubility of Cu2+ is very soil pH dependent and decreases 100-fold for each unit increase in pH. Plant uptake also decreases.

Fe

Ferric (Fe3+) and ferrous (Fe2+) activities in soil solution decrease 1000-fold and 100-fold, respectively, for each unit increase in soil pH. In most oxidized soils, uptake of Fe by crop plants decreases with increasing soil pH.

Mn

The principal ionic Mn species in soil solution is Mn2+, and concentrations decrease 100-fold for each unit increase in soil pH. In extremely acid soils, Mn2+ solubility can be sufficiently high to induce toxicity problems in sensitive crop species.

Mo

Above soil pH 4.2, MoO42− is dominant. Concentration of this species increases with increasing soil pH and plant uptake also increases. Water-soluble Mo increases sixfold as pH increases from 4.7 to 7.5. Replacement of adsorbed Mo by OH− is responsible for increases in water-soluble Mo as soil pH increases. Zinc solubility is highly soil pH dependent and decreases 100-fold for each unit increase in pH, and uptake by plants decreases as a consequence.

Zn Ni

Co

a

Ni2+ is relatively stable over wide ranges of soil pH and redox conditions. However, availability is usually higher in acidic than in alkaline soils. At pH 7 and higher, retention and precipitation increase. Increasing the pH of serpentine soils through liming from 4 to 7 reduced Ni in plant tissue. Solubility and availability of Co decrease with extreme soil pH. Presence of CaCO3, and high Fe, Mn, SOM, and moisture.

Adriano (1986), Fageria, Baligar, and Jones (1997), and Tisdale et al. (1985).

as influenced by soil pH and consequent acquisition by plants. Table V has been provided to show acquisition of Cu, Fe, Mn, and Zn by rice grown at various soil pH values. Boron is the only micronutrient to exist in solution as a nonionized molecule over soil pH ranges suitable for the growth of most plants. Increasing soil pH decreases B availability by increasing B adsorption onto clay and Al and Fe hydroxyl surfaces, especially at high soil pH (Keren and Bingham, 1985). The highest availability of B was at pH 5.5–7.5, and the availability decreased below or above this pH range. In other studies, B adsorption increased from pH 3 to 8 on kaolinite,

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MICRONUTRIENTS IN CROP PRODUCTION Table V Influence of Soil pH on Acquisition of Cu, Fe, Mn, and Zn by Upland Rice Grown in an Oxisol of Brazila Soil pH

Cu (μg plant−1)

Fe (μg plant−1)

Mn (μg plant−1)

Zn (μg plant−1)

4.6 5.7 6.2 6.4 6.6 6.8

75 105 78 64 61 51

4540 1860 1980 1630 1660 1570

11,160 5,010 4,310 3,610 2,760 2,360

1090 300 242 262 163 142

r2

0.89b

0.97c

0.99c

0.98c

a

Fageria (2000c). P < 0.05. c P < 0.01. b

montmorillonite, and two arid zone soils with peak adsorption at pH 8–10 and decreases from pH 10 to 12 (Goldberg, Forster, Lesch et al., 1996). Reduced B availability occurs from liming (called “B fixation”)(Fleming, 1980) as CaCO3 acts as an adsorption surface. As such, B deficiency may occur in plants grown in limed acid soils. Chloride is bound only lightly by most soil-exchange sites in acid to neutral soils and becomes negligible to pH 7.0. Chloride is easily leached from soil. Considerable soil Cu is specifically adsorbed as pH increases. For example, increasing the pH from 4 to 7 increased Cu adsorption (Cavallaro and McBride, 1984), and Cu was adsorbed on inorganic soil components and occluded by soil hydroxide and oxides (Martens and Westermann, 1991). Increases in soil pH above 6.0 induces hydrolysis of hydrated Cu which can lead to stronger Cu adsorption to clay minerals and OM. Readily soluble sources of Cu (exchangeable or sorbed) were highly toxic to citrus, and Cu concentrations decreased considerably with soil pH increases above 6.5 (Alva et al., 2000). Over-liming acid soils may also lead to Cu deficiency. SOM is a primary constituent for Cu adsorption and readily complexes Cu. As the pH increases, the sizes of organic colloids of high molecular weight diminish, thus increasing the surfaces where Cu can be adsorbed (Geering and Hodgson, 1969). The solubility of Fe decreases by ∼1000-fold for each unit increase of soil pH in the range of 4 to 9 compared to ∼100-fold decreases in the activity of Mn, Cu, and Zn (Lindsay, 1979). Iron exists in Fe0 (metallic), Fe2+ (ferrous), and Fe3+ (ferric) forms. Under acidic conditions, Fe0 readily oxidizes to Fe2+, and Fe2+ oxidizes to Fe3+ as the pH increases above 5. Ferric Fe (Fe3+) is reduced to Fe2+ and is readily

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available to plants in acidic soils, but precipitates in alkaline soils. Iron oxides are dominant in governing Fe solubility in soils. Minimum Fe solubility occurs between pH 7.5 and 8.5, which is the pH range of many calcareous soils (Lindsay, 1991). The increases in soil pH or Eh shift Fe from exchangeable organic forms to water-soluble and Fe oxide forms. The solubility of Fe in well-aerated soils is controlled by dissolution and precipitation of Fe3+ (Moraghan and Mascagni, 1991). Decreasing rhizosphere pH with added N (NH4–N) and/or K (KCl and/or K2SO4) was effective for increasing Fe uptake by plants (Barak and Chen, 1984). Applying FeSO4 with acid-forming fertilizer also increased Fe availability to plants (Moraghan and Mascagni, 1991). Soil pH affects solubility, adsorption, desorption, oxidation of Mn, and reduction of Mn oxides in soil. As the pH decreases, Mn is mobilized from various fractions and increases Mn soil solution concentrations and availability. Exchangeable Mn (plant available form) was high at low soil pH (<5.2), while organic and Fe oxide fractions of Mn (low availability form) were high at high pH (Sims, 1986). In sandy soil, increasing pH also increased organic fractions of Mn (Shuman, 1991). Increasing soil pH with Mg applications on peanut decreased Mn toxicity and leaf and stem Mn concentrations (Davis, 1996). The reduction of Mn4+ to Mn2+ is greatest at low soil pH, and acid soil conditions (<5) lead to Mn toxicities for many sensitive plant species (Mortvedt, 2000). In addition, high-molecular-weight organic colloids diminish as soil pH increases to increase surfaces where Mn as well as Cu and Fe can be adsorbed (Geering and Hodgson, 1969). Soil solution Mn increased 1.6-fold for each unit decrease in pH in a well-drained Mollisol acidified with high N fertilizer, indicating that soil acidity and aeration are important for Mn availability (Fageria and Gheyi, 1999). Manganese, Cu, and Fe are generally more available under conditions of restricted drainage or in flooded soils (Ponnamperuma, 1972). Molybdenum is the only micronutrient whose availability normally increases with increases in soil pH. The active form of Mo is normally MoO42−, which tends to polymerize when in solution. This condition is enhanced by acidification which could partially explain the low availability of Mo in some acid soils (KabataPendias and Pendias, 1984). The solubility of CaMoO4 and H2MoO4 (molybdic acid) increases with increases in soil pH. Molybdenum sorption on Fe oxides increased with decreases in soil pH in the range of 7.8 to 4.5 (Hodgson, 1963). Adsorption of Mo on Al and Fe oxides was maximum at pH <5, and decreased as the pH increased >5 with little or no adsorption at pH 8 (Goldberg, Forster, and Godfrey, 1996). Soil pH had pronounced effects on Mo adsorption between 3 and 10.5 with virtually no adsorption at pH 8 (Goldberg and Foster, 1998). Adsorption of Mo on hydrous Fe and Al oxides decreased as soil pH increased, and the addition of lime to soil normally increased Mo solubility and a cquisition by plants (Williams and Thornton, 1972). In addition, maximum Mo adsorption on Al and Fe oxides was at pH 4–5, but adsorption was maximum at pH 3.5 with

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humic acid and decreased as soil pH increased (Biback and Borggaard, 1994). Different mechanisms were apparent for Mo adsorption with humic acid compared to Al/Fe oxides, which involved complex formation between carboxyl and phenolic groups. Harmful effects occasionally arise for legumes grown in acid soils, as Mo deficiency may be more dominant than Al toxicity (Bohn et al., 1979). In some cases, both lime and Mo applications may be needed to provide adequate Mo to plants (Lindsay, 1991). Soil pH is more important than any other single property for controlling Zn mobility in soils (Anderson and Christensen, 1988). Increasing soil pH generally decreased Zn availability to plants (Saeed and Fox, 1977), and such decreases were usually due to higher adsorption of Zn. As soil pH increases above pH 5.5, Zn is adsorbed on hydrous oxides of Al, Fe, and Mn (Moraghan and Mascagni, 1991). However, the extent to which Zn is retained on Fe and Al hydrous oxides is influenced by the nature of clay minerals, surface conditions, and pH (Harter, 1991). In some cases, a soil pH higher than 7 may increase soil solution Zn due to solubilization of OM and also forms Zn(OH)+ and increased complexation of Zn with a lower positive charge (Barber, 1995). Gradual decreases in Zn activity as soil pH increases have been attributed to increased cation-exchange capacity (Stahl and James, 1991). Thirtyfold decreases in Zn concentration in acid soil have been reported for each unit increase in soil pH between 5 and 7 (McBride and Blasiak, 1979). Zinc was preferentially adsorbed over Cu on exchange sites indicating that chemisorption of hydrolyzed Zn occurs. Zinc adsorption is a major factor contributing to low concentrations of solution Zn in Zn-deficient soils. Soil pH affected Zn adsorption either by changing the number of sites available for adsorption or by changing the concentration of Zn species that is preferentially absorbed by plants (Barrow, 1986). Over-liming of soil may induce Zn deficiency and decrease Zn availability, especially at a high soil pH. Zinc absorption by wheat decreased as H+ concentrations increased, presumably because of the direct effects of H+ toxicity and the indirect effects of competition between Zn2+ and H+ for uptake sites on root surfaces (Chairidchai and Ritchie, 1993). The effect of pH may also be modified by organic ligands, and these ligands may decrease Zn uptake by plants as soil pH increases. Zinc deficiency may be expected in slightly acid and particularly in alkaline soils where inorganic Zn in equilibrium with soil Zn decreases between 10−8 and 10−10 M (Lindsay, 1991). Chemisorption of Ni on oxides, noncyrstalline alumino silicates, and layer silicate clays is favored at soil pH > 6, but exchangeable and soluble Ni 2+ is favored under lower pH conditions (McBride, 1994). The mobility of Ni is moderate in acid soils and becomes low in neutral and alkaline soils. Cobalt solubility decreases with increases in soil pH because of increased chemisorption on oxides and silicate clay, complexation by OM, and possible precipitation of Co(OH)2 (McBride, 1994). Cobalt is somewhat mobile in acid soils, but reduces as soil pH approaches neutrality.

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B. ORGANIC MATTER Soil OM may be grouped into water-insoluble (humic acids or humin) and water-soluble (fulvic acids and small molecular weight microbial products) compounds. Humic acids contain many anionic oxygen groups (phenolic hydroxyl and carboxyl, aliphatic carboxyl, alcoholic hydroxyl), which may interact with metal cations (Tate, 1987). Predominant reactions between humic acids and metals are ionic-bonding or complexation reactions. The increases in humification of OM increased these reactive groups and enhanced the potential for reaction with metallic cations (Stevenson, 1986). Metal complexation with humic substances normally forms strong metal complexes, while ionic bonding with low-molecular- weight organic acids (acetic, citric, malic) form relatively weak bonds. Both types of bonding normally result in the enhancement of metal mobility and/or plant availability (Tate, 1987), but some complexes are not readily available to plants (Harmsen and Vlek, 1985). Chemical reactions involved with SOM and metals have been reviewed (Stevenson, 1982). Native soil B was significantly and positively correlated with organic C (Elrashidi and O’Connor, 1982). Soil OM adsorbs B by ligand exchange and such adsorption is vital to B availability (Goldberg, 1997). Organic matter is the main source of B in acid soil, as relatively little B is adsorbed on mineral fractions at low pH. Born adsorption by soil-composed OM increases with increased SOM content and with increased soil pH (Yermiyahu et al., 1995). Even though reactions of B with OM are not well understood, B may be involved in reactions with hydroxyl groups on organic complexes (Offiah and Axley, 1993). Boron complexes with dihydroxyl compounds in OM, and these compounds retain considerable amounts of B (Marzadori et al., 1991). Soil OM also appears to be responsible for occluding important adsorption sites and reduces possible hysteretic reactions (confers reversibility characteristics) with adsorption sites (Marzadori et al., 1991). Because B is so closely associated with OM, it is usually more available in surface compared to subsurface soils because of higher amounts of OM in surface soil (Tisdale et al., 1985). Chloride bioavailability does not complex with and is not related to OM content in soil (Mortvedt, 2000). Copper is tightly bound to compounds in SOM, even more so than the other micronutrients, and is generally unavailable to plants (Mathur and Levesque, 1983). Much of the Cu in soil solution is also associated with OM (Kline and Rust, 1966). Low Cu levels in soil and Cu complexation into insoluble forms when soils have high OM lead to Cu deficiency in some plants (Moraghan and Mascagni, 1991). The major portions of total Cu were organically bound in an acid sandy soil, but precipitated when soil pH was high (Alva et al., 2000). The solubility of Cu in soil is usually decreased by complexation with clay–humus particles and/or formation of insoluble humic complexes (Stevenson and Fitch, 1981). In Cu-deficient soils,

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humic and fulvic acids probably form highly stable complexes with Cu to reduce its availability. Complexation of Cu with OM occurs mainly at solution pH values above 6.5 (Barber, 1995), and increased Cu complex formation usually occurs with increased pH, decreased ionic strength, and increased OM/Cu ratios (Sanders and Bloomfield, 1980). Inorganic Cu commonly complexes with hydroxyls and carbonates when soil solution pH is >7.0 (McBride, 1981). The breakdown of crop residues by soil microbes may release significant amounts of Cu, but natural complexing substances produced during OM decomposition could complex Cu into unavailable forms (Moraghan and Mascagni, 1991). Iron forms stable complexes with organic compounds that occur in both soil and solid phases (Barber, 1995). Organic acids such as citric, malic, oxalic, and phenolic that form soluble Fe complexes are released when OM decomposes. These Fe complexes enhance the mobility and bioavailability of Fe (Lindsay, 1991). Even though Fe complexes with OM, Fe bioavailability is affected more by soil pH than by OM content. Fulvic and humic ligands form the most stable complexes with Fe compared to the other transition metals, and the effectiveness of these complexes increases with increasing pH because of the enhanced dispersion and ionization of surface ligands (Stevenson, 1991). The formation of soluble Fe complexes by naturally occurring chelating ligands may also increase Fe solubility in soil. The addition of OM to soil leads to reducing conditions, and Fe is changed from less soluble to exchangeable and organic forms under these conditions (Shuman, 1991).The biological degradation of OM also releases electrons or other reducing agents to lower soil redox potentials and significantly increases the solubility of Fe (Lindsay, 1991). Increases in oxalate-extractable Fe (and Al) occurred after decomposition of OM, and Fe and Al oxide adsorption sites became coated or occluded with OM and were active only after removal of OM (Marzadori et al., 1991). In addition, Fe availability improved with the addition of OM in drained and water-logged soils (Tisdale et al., 1985). Soil OM content has been related to increased, decreased, and no effects on Mn availability to crop plants (Reisenauer, 1988). Within soil fractions, exchangeable and organically bound forms of Mn are important to plant availability. The higher accumulation of Mn in surface soil horizons has been reported to indicate that Mn may be closely associated with OM (McDaniel and Buol, 1991). Positive correlations between OM and Mn indicate that Mn has a strong affinity for OM, and higher Mn concentrations in surface soil compared to lower layers are likely due to higher OM in surface horizons (Zhang et al., 1997b). Sites of Mn retention have also been associated not only with OM but also with CaCO3 in pH 8 calcareous soils (Karimian and Gholamalizadeh Ahangar, 1998). Mn2+ especially forms complexes with fulvic and humic acids and humins, and with organic ligands such as organic, amino, and sugar acids, hydroxamates, phenolics, siderophores, and other organic compounds produced by various organisms in soil solution (Marschner, 1995; Stevenson, 1986; Tate, 1987). Hydrated Mn2+ forms complexes with carboxyl

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groups of OM, which helps explain observations that Mn binds weakly to OM compared to Fe, Cu, and Zn (Bloom, 1981). Manganese availability in soils high in OM may also decrease because of the formation of unavailable Mn complexes. Unavailable Mn complexes form in peaty or muck soils. Soil OM appears to have smaller effects on the availability of Mo than does soil pH. Molybdenum availability under acid soil conditions is primarily affected through the adsorption of MoO42− onto inorganic soil components. However, evidence exists that Mo is fixed by OM (Moraghan and Mascagni, 1991). In southeastern United States soils, adsorbed Mo increased with increases in SOM and Fe–oxide contents (Karimian and Cox, 1978). Organic matter may also potentially increase the mobilization of Mo under conditions of impeded drainage. Soil OM appears to affect the availability of Zn by (i) increasing the solubility of Zn through the formation of complexes with organic, amino, or fulvic acids; (ii) forming insoluble Zn–organic complexes that decrease the solubility of Zn; (iii) roots releasing exudates and ligands that may complex Zn in the rhizosphere; and (iv) microbes immobilizing and mineralizing decreased or increased soilavailable Zn (Lindsay, 1972). Increased levels of OM increase exchangeable and organic fractions of Zn and decrease oxide fractions of Zn in soil because of reducing conditions to enhance Zn bioavailability. A widespread Zn deficiency in lowland rice in Asia was related to high soil pH, low available soil Zn, and OM content (Yoshida et al., 1973). The decomposition of OM releases OH−, HCO3−, and organic ligands that tend to immobilize Zn in the root rhizosphere (Yoon et al., 1975). In practice, fine-textured soils and soils with horizons containing high levels of OM had higher Zn sorption capacities than sandy-textured, low OM soils (Stahl and James, 1991). Adsorption of organic anions may also increase negative charges on particle surfaces to enhance Zn adsorption. On the other hand, organic ligands in solution may decrease Zn adsorption by competing with surface sites for Zn. Zinc adsorption onto clays and hydrous oxides may be increased or decreased with organic ligands (Chairidchai and Ritchie, 1990). High SOM levels in Ni-rich soils can solubilize Ni2+ as organic complexes at high soil pH (McBride, 1994). At high soil pH, Co complexes with SOM, and Co bioavailability increases when it is complexed with SOM (McBride, 1994).

C. TEMPERATURE, MOISTURE, AND LIGHT Temperature and moisture are important factors affecting the availability of micronutrients in soils (Cooper, 1973; Fageria, Baligar, and Jones, 1997). The availability of most micronutrients tends to decrease at low temperatures and moisture contents because of reduced root activity and low rates of dissolution and diffusion of nutrients. In soils with low moisture, colloidal particles may become immobilized as a result of micronutrient adsorption on surfaces of soil particles (Harmsen and Vlek, 1985). Light affects mostly metabolic processes of plants.

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Boron and Cl uptake are influenced more than any other mineral for plants grown under hot and dry conditions. For example, increased temperatures in nutrient solutions enhanced B concentrations in shoots of plants by increasing B uptake with increased transpiration (Moraghan and Mascagni, 1991; Vlamis and Williams, 1970). On the other hand, turnip was B deficient when grown in soil with <0.3 mg B kg−1 of hot water-extractable B, but became B deficient when grown in the field with 0.5–0.6 mg kg−1 hot water-extractable B during a dry summer (Batey, 1971). The availability of B decreases under drought conditions most likely because of the reduced mobility of B by mass flow to roots (Barber, 1995). Boron can move relatively long distances by mass flow and diffusion to roots. Soil drying reduces B diffusion by reducing the mobility of soil solution and increasing the diffusion path length (Scott et al., 1975). Boron deficiency in crops commonly occurs during drought periods because of restricted water flow to roots, and B deficiency may also restrict root growth to reduce acquisition of water and intensify drought stress effects (Bouma, 1969). The lack of soil moisture reduces the rate of transpiration, thereby reducing B transport to shoots (Lovatt, 1985). Wetting and drying cycles and increasing soil temperature (e.g., 25 to 45◦ C) also increased B fixation by montmorillonitic and kaolinitic clays (Biggar and Fireman, 1960). Low temperature in spring and fall seasons of temperate regions reduced availability of B to forage legumes, while increased temperature enhanced B concentrations for sugarcane (Gupta, 1993). Another aspect of drought-induced B deficiency involves moisture stress that may restrict the mineralization and availability of organically bound soil B (Evans and Sparks, 1983; Flannery, 1985). High light intensity may also induce B deficiency and reduce B toxicity (Moraghan and Mascagni, 1991). Temperature can affect mobilization/immobilization reactions to decrease/ increase solubility of organically bound soil Cu and its acquisition by plants (Moraghan and Mascagni, 1991; Stevenson and Fitch, 1981). For example, increasing temperature from 8 to 20◦ C increased Cu uptake by carrot grown in acid organic soil (MacMillan and Hamilton, 1971). Soil moisture had no consistent effect on Cu levels available to alsike clover (Kubota et al., 1963), but Cu availability to annual ryegrass increased when roots had access to subsoil water (Nambiar, 1977). Flooding soil also decreased Cu availability to rice (Beckwith et al., 1975). Low Cu acquisition by plants was attributed to low soil moisture conditions in the zone of Cu application (Mortvedt, 2000). Iron deficiency, which occurs predominantly in calcareous and alkaline soils, is commonly enhanced by low soil temperature and high water (wet) and/or poorly aerated conditions (Marschner, 1995). Low soil temperatures reduce root growth and metabolic activity and increase HCO3− levels in the soil solution to increase the severity of Fe deficiency with the increased solubility of CO2 in soil solutions (Inskeep and Bloom, 1986). On the other hand, high soil temperature may decrease Fe acquisition by increasing the microbial decomposition of organic materials to stimulate microbial activity and CO2 production to increase the severity of Fe

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deficiency (Inskeep and Bloom, 1986; Moraghan and Mascagni, 1991). High aerial or soil temperatures may also stimulate relative growth rates to enhance the induction of Fe deficiency (Inskeep and Bloom, 1986). High soil temperature may also increase P uptake to enhance P-induced Fe deficiency (Moraghan and Mascagni, 1991). Since absorption of Fe by plant roots is largely restricted to actively growing root tips, restricted root growth in dry surface layers (zone with highest amount of available Fe) may partially explain the appearance of Fe deficiency for some plants grown under hot, dry conditions (Moraghan and Mascagni, 1991). Soil temperature generally has less effect on Fe deficiency in Strategy II (root release of phytosiderophores) than in Strategy I (root release of organic acids and increased root reducing power) plants (R¨omheld and Marschner, 1986). Increasing light intensity enhanced the release of phytosiderophores by cereal roots, which could increase uptake of both Fe and Zn (Cakmak et al., 1998). Drying and flooding of acid sulfate soils increase the risk of Fe toxicity (Sahrawat, 1979), since water-logging enhances the accumulation of high amounts of soluble Fe2+, especially in acid soils. Good soil drainage increases oxidation, and Fe toxicity in rice is commonly reduced (Gunawardena et al., 1982). The ratio of Fe2+/(Fe2+ + Mn2+ + Ca2+ + Mg2+) in the soil solution, rather than the activity of Fe2+ alone, controlled Fe acquisition by flooded rice grown in the acid sulfate soils of Thailand (Moore and Patrick, 1989). High levels of Mn, Ca, and Mg also reduced the likelihood of Fe toxicity for plants grown in acid soils. Low soil temperature may induce Mn deficiency. For example, Mn deficiency of field-grown soybean was more severe at low temperature despite having high Mn concentrations in shoot tissue (Ghazali and Cox, 1981). Critical Mn concentrations in leaves are often lower at low than at high soil temperatures (Rufty et al., 1979). High soil temperatures may increase the solubility of soil Mn and enhance the Mn availability, and air drying often combined with high temperature increased extractable and exchangeable Mn, which sometimes has led to Mn toxicity (Moraghan and Mascagni, 1991). Soil temperature increases of 10 to 25◦ C approximately tripled Mn accumulation in shoots of barley grown in organic soil (Reid and Racz, 1985), while soybean grown at 16, not 24◦ C, developed severe Mn toxicity symptoms when grown in calcareous soil (Moraghan et al., 1986). Plant tolerance to Mn toxicity increased in tobacco and soybean with increased temperatures despite higher Mn absorption, which was attributed to faster plant growth to provide larger leaf vacuoles to sequester potentially toxic Mn (Heenan and Carter, 1976; Rufty et al., 1979). Excess moisture favors Mn-reducing conditions and water-logging, even for relatively short periods of time, and enhanced Mn accumulation could possibly induce Mn toxicity (Moraghan and Mascagni, 1991; Siman et al., 1974). Excess soil moisture can restrict diffusion of O2 within soils and favor Mn reduction. At lower soil redox potentials, high levels of Fe2+ may also be formed which could lead to Mn–Fe antagonisms (Vlamis and Williams, 1962, 1964). Manganese deficiency

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has rarely been observed in rice grown under flooded conditions, and Mn toxicity was aggravated in alfalfa grown under hot dry conditions in Australia (Siman et al., 1974). Manganese deficiency on various crops in Sweden disappeared after a heavy rainfall following a dry period (Stahlberg and Sombatpanit, 1974). High and low light intensities may intensify Mn deficiency and toxicity symptoms on plants (Hewitt, 1966). High intensity stimulated Mn absorption and accentuated the severity of Mn toxicity (El-Jaoual and Cox, 1998; Horiguchi, 1998). The Mn-induced chlorosis symptoms on leaves with high light intensity were attributed to the oxidation of chlorophyll (El-Jaoual and Cox, 1998). On the other hand, decreased light intensity appeared to lower Mn concentrations in leaves through reduced water transport and increased the leaf area to dilute internal Mn (Campbell and Nable, 1988). Molybdenum is associated with N2 fixation, and low temperatures will suppress this process and lower Mo requirements (Anderson, 1956). The temperature had little effect on plant incidence or severity of Mo deficiency (Moraghan and Mascagni, 1991). The adsorption of Mo increased when the temperature increased from 10 to 40◦ C (Goldberg and Forster, 1998). The acquisition of Mo decreased in plants grown under dry conditions (Gupta and Sutcliffe, 1968). Submerged acid soils had increased soluble Mo fractions because of decreased MoO42− adsorption (Ponnamperuma, 1972). Temperatures lower than optimum normally decrease Zn acquisition by crop plants. Zinc deficiency symptoms were relatively severe at low soil temperature, but Zn concentrations increased when the temperature was increased (Martin et al., 1965). Added P also induced Zn deficiency at low soil temperature. Cool and wet conditions induced Zn deficiency, which were related to reduced mineralization of Zn and reduced root growth (Moraghan and Mascagni, 1991). Spring-seeded crops like maize, edible bean, and potato grown in western United States soils exhibited early season Zn deficiency symptoms, which did not appear in newer growth later in the season (Viets, 1967). The detrimental effects of low root temperatures on Zn accumulation by maize grown in nutrient solution were partially due to decreased translocation from roots to shoots (Edwards and Kamprath, 1974). Since Zn moves to roots mainly by diffusion, Zn deficiency is common also in crops grown under dry conditions (Warncke and Barber, 1972). Mycorrhizae associated with roots enhances uptake of Zn (Clark and Zeto, 2000), and low soil temperatures may severely reduce root colonization with mycorrhizae and induce Zn deficiency (Hayman, 1974). Zinc deficiency was less severe for plants grown under low light and cool conditions compared to optimum growth conditions (Moraghan and Mascagni, 1991). Zinc deficiency frequently associated with flooded soil may be the result of Zn reactions with free sulfide (Sajwan and Lindsay, 1988). Under flooded conditions, Zn may precipitate as ZnS or possibly form organic–Zn complexes which can lead to reduced availability. Zinc may also react with sesquioxides under flooded

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conditions to enhance Zn deficiency (Sajwan and Lindsay, 1986). Added OM also suppressed Zn acquisition due to redox processes and buildup of Fe2+ (Giordano et al., 1974). Flooding–drying and alternating wetting–drying decreased Zn adsorption, whereas preflooding increased Zn adsorption, and the addition of OM increased Zn adsorption under these water treatments (Mandal and Hazra, 1997). Under reducing conditions Ni2+ is incorporated into sulfides that restrict its mobility to very low levels, and strong oxidizing soil conditions favor adsorption of Co (McBride, 1994).

IV. FACTORS ASSOCIATED WITH SUPPLY AND ACQUISITION Sufficient concentrations and/or available forms of micronutrients must be at or near root surfaces to meet plant acquisition needs. Nutrient supplies to plants are governed by such factors as concentrations inside plants and in soil solution, supply and chemistry at root surfaces or in the rhizosphere, and interactions of one nutrient with another. At any given time, concentrations of nutrients in the solution immediately adjacent to roots appear to be one of the best measures for assessing absorption potential, although plant and rhizosphere factors may influence the rates of absorption (Fageria, Baligar, and Wright, 1997). Information about mechanisms and processes associated with mineral nutrient uptake and translocation are not discussed here, since many review articles are available on the subject (Barber, 1995; Clarkson and Hanson, 1980; Fageria, Baligar, and Jones, 1997; Glass, 1989; Kochian, 1991; Marschner, 1995; Moore, 1972; Tiffin, 1972). This article will focus on supply and general acquisition processes.

A. DEFICIENCIES AND TOXICITIES For plants to obtain micronutrients for proper physiological and biochemical functioning (Table VI), these mineral nutrients need to be at appropriate concentrations. Micronutrient deficiencies and toxicities are widespread and have been documented in various soils throughout the world. The deficiency of essential micronutrients induces abnormal pigmentation, size, and shape of plant tissues, reduces leaf photosynthetic rates, and leads to various detrimental conditions (Masoni et al., 1996). Specific deficiency symptoms appear on all plant parts, but discoloration of leaves is most commonly observed. Deficiency symptoms of low mobile nutrients (Fe, B, Mn, Zn, and Mo) appear initially and primarily on upper leaves or leaf tips, while symptoms of mobile nutrients (N, P, K, and Mg) appear primarily on lower leaves. Deficiency and toxicity symptoms may be confused

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Table VI Functions of Micronutrients in Plantsa Element B Cl Cu

Fe

Mn Mo Zn Ni Co

Function Activates certain dehydrogenese enzymes. Involved in carbohydrate metabolism. Synthesis of cell wall components. Essential for cell division and development. Essential for photosynthesis and as an activator of enzymes. Involved in splitting water. Functions in osmoregulation of plants growing on saline soils. Constituent of a number of important oxidase enzymes including cytochrome oxidase, ascorbic acid oxidase, and lactase. Important in photosynthesis and protein and carbohydrate metabolism. Important in chlorophyll formation and an essential component of several peroxidase, catalase, and cytochrome oxidase enzymes. Found in key metabolic functions such as N2 fixation, photosynthesis, and electron transfer. Activates decarboxylase, dehydrogenese, and oxidase enzymes. Involved in photosynthesis, N metabolism, and assimilation. An essential component of nitrate reductase and N2-fixation enzymes and required for normal assimilation of N. Essential component of several dehydrogenase, proteinase, and peptidase enzymes. Promotes growth hormones, starch formation, and seed maturation. Component of urease enzyme. Participates in redox reactions. Improves hydrogenase acitivity, urea hydrolysis. Stimulates germination and growth. Nodule development, rhizobium infection, N2 fixation, component of coenzyme cobalamin (vitamin B12).

a From Brady and Weil (1996), Fageria, Baligar, and Jones (1997), Marschner (1995), and Stevenson (1986).

with drought, disease, insect, and other damage, so correct diagnosis may be difficult without experience. Critical concentration ranges of micronutrients in soil for important field crops (Table VII) and some description of deficiency and toxicity symptoms associated with many crop plants (Table VIII and Table IX) have been provided. Boron deficiency is common for plants grown in arid, semiarid, and heavy rainfall areas in calcareous, sandy, light textured, acid, and low OM soils (Bradford, 1966; Gupta, 1993). Soils supplied with high amounts of municipal compost, sludge, and biosolids tend to accumulate high amounts of B which may result in B toxicity. Boron toxicities are commonly associated with crops receiving irrigation water containing high B. Differences between B sufficiency and toxicity are narrow (Marschner, 1995). Chlorine deficiencies under field conditions have been reported for oil palm, sugarcane, hard red spring wheat, and potato (Martens and Westermann, 1991). Soybean grown in Atlantic coastal plain soils with added KCl developed Cl

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FAGERIA et al. Table VII Critical Micronutrient Concentrations (mg kg−1) in Soil for Some Field Cropsa Critical concentration Element B

Crop

Cl

Alfalfa, sugar beet, cotton, maize, peanut Wheat, barley, oat

Cu

Maize and small grains Barley and oat Rice Maize, soybean and wheat

Fe Mn

Mo

Zn

Sorghum and soybean Sorghum Soybean Small grains Maize Soybean Forage legumes, Soybean, Cauliflower Bean (common), maize, rice, sorghum, flax Maize Maize Rice

Extracting solution

Range

Mean

Hot water

0.1–2

0.8

Water 0.01 M Ca(NO3)2 0.05 M K2SO4 CaO NH4HCO3–DTPA Mehlich-1 0.05 M EDTA 0.05 M HCl Mehlich-1 NH4HCO3–DTPA Mehlich-3 NH4HCO3–DTPA DTPA–TEA Mehlich-1 NH4HCO3–DTPA Mehlich-3 Mehlich-3 NH4–oxalate

NH4HCO3–DTPA Mehlich-1 0.1 M HCl DTPA–TEA 0.05 M HCl

>22

0.12–2.5 0.1–10

2.5–5 4–8 1–2

0.8 3 1.1 0.1 0.26 0.53 0.37 4.8 4.5 7 1.4 3 3.9

0.1–0.3

0.25–2 0.5–3 2–10

0.8 1.1 5 0.86 1

a

From Cox (1987), Martens and Lindsay (1990), Sims (2000), and Sims and Johnson (1991).

toxicity (Parker et al., 1983). Crops that are grown in salt-affected soils and receive irrigation (sprinkler) often have enhanced symptoms of Cl toxicity. Copper deficiency is often observed on plants grown in soils inherently low in Cu (coarse-textured and calcareous soils) and in soils high in OM, where Cu is readily complexed (Alloway and Tills, 1984). Higher than normal Cu supplies usually inhibit root growth more than shoot growth (Lexmond and Vorm, 1981). The use of Cu-containing fungicides and antihelminthic compounds (insecticides) in agriculture has resulted in Cu toxicity in some plants, but naturally occurring Cu toxicity is relatively uncommon (Welch et al., 1991).

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Table VIII Micronutrient Deficiency Symptoms in Crop Plantsa Element B Cl Cu Fe Mn

Mo

Zn

Ni Co

Symptoms Death of growing points of shoot and root. Failure of flower buds to develop. Blackening and death of tissues, especially inner tissue of brassica plants. Reduced leaf size. Yellowing, bronzing and necrosis on leaves. Roots reduced in growth and without hairs. Yellowing of young leaves. Rolling and dieback of leaf tips. Leaves are small. Tillering is retarded. Growth is stunted. Interveinal yellowing of younger leaves with distinct green veins. Entire leaves become dark yellow or white with severe deficiency, and leaf borders turn brown and die. Interveinal tissue becomes light green with veins and surrounding tissue remaining green on dicots (Christmas tree design) and long interveinal leaf streaks on cereals. Develop necrosis in advanced stages. Mottled pale appearance in young leaves. Bleaching and withering of leaves and sometimes tip death. Legumes suffering Mo deficiency have pale green to yellowish leaves. Growth stunted. Seed production is poor. Deep yellowing of whorl leaves (cereals). Dwarfing (rosette) and yellowing of growing points of leaves and roots (dicots). Rusting in strip on older leaves with yellowing in mature leaves. Leaf size reduced. Main vein of leaf or vascular bundle tissue becomes silver-white, and marked stripes appear in middle of leaf. Chlorosis of newest leaves. Ultimately leads to necrosis of meristems. Reduced germination and seedling vigor (low seed viability). Diffuse yellowing in leaves. Young shoots and older leaves have severe localized marginal scorching.

a From Baligar et al. (1998), Bennett (1993), Bould et al. (1983), Brown et al. (1987), Clark and Baligar (2000), and Fageria, Baligar, and Jones (1997).

Iron deficiency is a worldwide problem and occurs in numerous crops (Korcak, 1987; Marschner, 1995; Vose, 1982). Iron deficiency occurs not because of Fe scarcity in soil but because of various soil and plant factors that affect Fe availability to inhibit its absorption or impair its metabolic use (Marschner, 1995; Welch et al., 1991). In the majority of soils, the total concentration of soluble Fe in the rhizosphere is nearly always far below the level required for adequate plant growth (Marschner, 1995). Induced Fe-deficient chlorosis is widespread and is a major concern for plants growing on calcareous or alkaline soils due to their high pH and low Fe (Korcak, 1987). Bicarbonate, nitrate, and environmental factors influence the occurrence of Fe-deficient chlorosis in plants, which occurs in young leaves due to inhibited chloroplast chlorophyll syntheses as a consequence of the low Fe nutrition status of plants (Lucena, 2000). Plant species that commonly become Fe deficient are apple, peach, citrus, grape, peanut, soybean, sorghum, and upland

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FAGERIA et al. Table IX General Description of Mineral Toxicity Symptoms on Plantsa

Element B

Cl Cu

Fe

Mn

Mo Zn

Ni

Co

Symptoms High B may induce some interveinal necrosis, and severe cases turn leaf margins straw color (dead) with distinct boundaries between dead and green tissue. Roots appear relatively normal. High Cl results in burning leaf tips or margins, reduced leaf size, sometimes yellowing, resembles K deficiency, and root tips die. High Cu may induce Fe deficiency (chlorosis). Light colored leaves with red steaks along margins. Plants become stunted with reduced branching, and roots are often short or barbed (like wire). Laterals may be dense and compact. Excess Fe is a common problem for plants grown in flooded acidic soil. May induce P, K, and Zn deficiencies. Bronze or blackish-straw colored leaves extending from margins to midrib. Roots may be dark red and slimy. Excess Mn may cause leaves to be dark green with extensive reddish-purple specks before turning bronze yellow, especially interveinal tissue. Uneven distribution of chlorophyll. Margins and leaf tips turn brown and die. Sometimes Fe deficiency appears, and main roots become stunted with increased number and density of laterals. Excess Mo induces symptoms similar to P deficiency (red bands along leaf margins), and roots often have no abnormal symptoms. Excess Zn may enhance Fe deficiency. Leaves become light colored with uniform necrotic lesions in interveinal tissue, sometimes damping off near tips. Roots may be dense or compact and may resemble bared wire. High Ni results in white interveinal banding alternating with green semichlorotic areas with irregular oblique streaking, dark green veins, longitudinal white stripes, and brown patches. Yellowing of leaves may resemble Fe or Mn deficiency. Distortion of young leaflets (peg-like or hook type). Pale green leaves with pale longitudinal stripes.

a From Baligar et al. (1998); Bould et al. (1983); Clark and Baligar (2000), and Fageria, Baligar, and Jones (1997).

rice. Iron toxicity (bronzing) can be a serious disorder for the production of crops in water-logged soils. For wetland rice, Fe toxicity is the second most severe yield-limiting mineral disorder after P deficiency. Audebert and Sahrawat (2000) reported that the application of P, K, and Zn with N to an iron-toxic lowland soil in the Ivory Coast reduced Fe toxicity symptoms and increased lowland rice yields. Manganese toxicity is probably more of a problem than Mn deficiency throughout the world. Manganese deficiency occurs on plants grown in organic, alkaline, calcareous, poorly drained, slightly acid soils, and coarse-textured sandy soils (Martens and Westermann, 1991). Over-liming of acid soils may induce Mn deficiency. Manganese toxicity is a major factor for reduced production of crops grown in acid soils, as is Al toxicity. Plant ability to tolerate Mn toxicity is affected by plant genotype, concentration of Si in soils, temperature, light intensity,

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and physiological age of leaves (Horst, 1988). The conditions that lead to the buildup of high levels of Mn in soil solution are high levels of total Mn, soil pH below 5.5, high soluble Mn relative to Ca, reduction of Mn under low oxygen caused by poor drainage, soil compaction, and excess water from irrigation or rainfall (Reisenauer, 1988). Molybdenum deficiency is widespread in legumes, maize, and cauliflower grown in acid mineral soils containing high amounts of iron oxides and hydroxides. Copper/Mo ratios <2 will normally reduce Mo deficiency in plants (Miltmore and Mason, 1971). The appearance of Mo toxicity is rare, but high levels of Mo in forages may induce Cu deficiency in animals. Molybdenum concentrations >5 to 10 mg kg−1 dry wt in forage tissue have induced toxicity in ruminants (“molybdenosis or teart”) (Marschner, 1995). Such disorders of Cu occur in forage grown in poorly drained and high organic soils. Zinc deficiency in plants is widespread throughout the world (Bould et al., 1983; Viets, 1966). Increasing pH due to liming reduces plant available Zn. High clay and P supply and low soil temperatures are also known to promote Zn deficiency (Marschner, 1995). Lowland rice grown in limed or calcareous soils often exhibit Zn deficiency (Ponnamperuma, 1972). Chaney (1993) indicated that after “natural” phytotoxicity from Al or Mn in strongly acid soils, Zn phytotoxicity is the next most extensive micronutrient phytotoxicity compared to Cu, Ni, Co, Cd, or other trace element toxicities. As soil pH decreases, Zn solubility and uptake increase, and the potential for Zn phytotoxicity increases. At comparable soil pH and total Zn contents, Zn phytotoxicity is more severe on plants grown in light-textured than in heavy-textured soils. This is mainly because of the differences in the specific Zn adsorption capacities of soil. Continued applications of Zn to alkaline sandy soils low in OM and clay tend to develop Zn toxicity in plants, even though the occurrence of Zn toxicity is relatively rare under field conditions (Rattan and Shukla, 1984). Liming was effective in overcoming Zn toxicity on peanut (Keisling et al., 1977). Even though no clear evidence exists for Ni deficiency in plants, Ni toxicity is of concern for plants grown in soil receiving sewage sludge and industrial by-products. Nickel as well as Co toxicity may also be found on plants grown in soils formed from serpentinite or other ultrabasic rocks (McBride, 1994). Cobalt deficiency may occur on plants grown in highly leached sandy soils derived from acid igneous rocks and in calcareous or peaty soils (Martens and Westermann, 1991) and in coarse-textured, acid-leaching alkaline or calcareous soils and humic rich soils (McBride, 1994).

B. SUPPLY AND UPTAKE Micronutrient uptake by roots depends on nutrient concentrations at root surfaces, root absorption capacity, and plant demand. Micronutrient acquisition includes dynamic processes in which mineral nutrients must be continuously

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FAGERIA et al. Table X Estimated Proportions of Micronutrients Potentially Supplied by Mass Flow, Diffusion, and Root Interception to Maize Roots Grown in a Fertile Alfisola Estimated percentage of total uptake Micronutrient

Mass flow

Diffusion

Root interception

B Cu Fe Mn Zn

1000 219 66 22 230

29 0 21 35 0

29 6 13 43 43

a

From Barber (1966).

replenished in soil solution from the soil solid phase and transported to roots as uptake proceeds. Mineral nutrient transport to roots, absorption by roots, and translocation from roots to shoots occur simultaneously, which means that rate changes of one process will ultimately influence other processes involved in uptake (Fageria, Baligar, and Jones, 1997). In soil systems, mineral nutrients move to plant roots by mass flow, diffusion, and root interception (Barber, 1995). Mass flow is the passive transport of minerals to roots as water moves through soil and occurs when solutes are transported to roots with convective flow of water (soil solution) from soil. The amount of minerals supplied to roots depends on the rates of water flow to roots and the average mineral content of the water. The amounts of mineral nutrients reaching roots by this process depend on the concentrations of nutrients in soil solution and the rates of water transport to and into roots. Diffusion and mass flow could meet plant micronutrient requirements for B, Cu, and Zn, provided sufficient nutrient concentrations are in soil solution. Table X provides estimates of nutrients supplied to maize roots by mass flow, diffusion, and root interception in a fertile Alfisol. Diffusion is defined as the movement of nutrients from regions of high concentration to regions of low concentration. When the nutrient supply to root surfaces is not sufficient to satisfy plant demands by mass flow and root interception, concentration gradients develop and nutrients move by diffusion (Barber, 1966, 1995). Considerable quantities of B, Mn, and Fe move by diffusion. Root interception is another process by which roots obtain minerals. As roots grow in soil, they push soil particles aside and root surfaces come in direct contact with mineral nutrients. Mineral interception by roots depends on soil volume occupied by roots, root morphology, and concentrations of minerals in the soil volume occupied by roots. On average, soil volume occupied by roots of crop

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plants is about 0.7 to 0.9% (Fageria, Baligar, and Wright, 1997). Root interception can provide significant amounts of plant requirements for B, Zn, and Mn. The interaction of soil and plant factors influences the processes of mineral flux in soil. The major soil factors that influence mineral flux are concentrations of mineral ions on exchange sites and in solution, soil buffer capacity, diffusion coefficient, type of clay, soil structure, nature of OM, water content, and temperature. Soil capacity to adsorb mineral nutrients is important in mineral transport to roots. If soil ion-exchange capacity is low, ions are usually freely mobile in solution. In addition, diffusion coefficients of Cu, Mn, and Zn decrease ∼10-fold for various clays in the order of kaolinite > illite > montmorillonite > vermiculite (Lindsay, 1979). The major plant factors that contribute to mineral fluxes are root and root hair density and length, plant demand for mineral nutrients and water, and plant modification of the rhizosphere (Fageria and Baligar, 1993, 1997a,b). The amount of minerals in soil, concentration in soil solution, and transport to roots are key factors influencing mineral uptake by roots. Since B, Mn, and Fe move to plant roots primarily by diffusion, soil properties that affect diffusion govern micronutrient availability to plant roots. Mineral nutrient supply, whether at adequate or toxic levels, can strongly influence root growth, morphology, and distribution of root systems in soil (Baligar et al., 1998; Barber, 1995; Marschner 1995). As most micronutrients may be supplied by diffusion, the size of roots has profound effects on plant ability to acquire required mineral concentrations. Toxic levels of Al, Mn, and H in acid soils and the presence of H2CO3, Na2CO3, B, Na, Mo, SO4–S, and Cl in alkaline or high-salt soils can directly reduce root growth and inhibit ability of roots to explore large soil volumes for minerals and water. Soil weathering, anthropogenic activities, addition of agricultural amendments (fertilizers, organic manures, lime, slags, sewage sludge), and pesticides have contributed to increased levels of essential micronutrients and nonessential trace elements in soil (Baligar et al., 1998). The mobility and bioavailability of these minerals in soil are influenced by pH, temperature, redox potential, cation exchange, anion ligand formation, and composition and quantity in soil solution (Alloway, 1995a,b; Baligar et al., 1998). At any given pH, the relative mobility of some micronutrients in acid soil decreases in the order of B > Ni > Zn > Mn > Cu. Mineral nutrient deficiencies and excesses affect growth (dry mass, root : shoot ratio) and morphology (length, thickness, surface area, density) of roots and root hairs (Baligar et al., 1998). Nutrient deficiencies usually lead to finer roots and trace element toxicities stimulate initiation and growth of second- and third-order lateral roots, while tap roots and first-order laterals (seminal/basal) become suppressed (Hagemeyer and Breckle, 1996). Additional information about toxicity and constraints of micronutrients and trace elements on root growth is available (Baligar et al., 1998). Changes in root growth and morphology affect plant ability to absorb minerals from soil to meet plant demands. Mineral uptake involves selectivity [where certain minerals are absorbed preferentially over others

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(discrimination or exclusion)], accumulation (where minerals accumulate at higher concentrations in cell sap than in external soil solution), and genotype (where distinct differences exist among plant species and within species) (Marschner, 1995). A detailed discussion and reviews of plant and soil factors that affect micronutrient uptake, transport, and utilization in plants are available (Barber, 1995; Chen and Hadar, 1991; Graham et al., 1988; Gupta, 1993; Marschner, 1995; Mengel and Kirkby, 1982; Mortvedt et al., 1991; Robson, 1993; Sumner, 2000; Welch, 1995). Micronutrient cations in soil solution also commonly form organic complexes of varying stability, size, and charge (Tiffin, 1972). Kochian (1991) stated that to understand the overall mechanisms of micronutrient cation uptake in plants there is a need to consider the form of metal chelates in the root rhizosphere at the root–cell plasma membrane, forms of micronutrient cations transported into plant cells, and the nature of the metal chelate complexes, both within cells and involved in long-distance transport. A detailed discussion of the processes associated with mineral uptake and transport is provided in several review articles (Epstein, 1972; Kochian, 1991; Marschner, 1995; Moore, 1972; Mengel and Kirkby, 1982; Tiffin, 1972). Boron is absorbed by roots as undissociated boric acid [B(OH)3 or H3BO3], and it is not clear whether uptake is active or passive (Marschner, 1995; Mengel and Kirkby, 1982). Nevertheless, B uptake by rice appeared to be passive under normal B supplies and active under low B supplies (Yu and Bell, 1998) and was the result of passive assimilation of undissociated boric acid (Hu and Brown, 1997). At high B supplies, passive uptake and active excretion of B were also noted (Yu and Bell, 1998). Boron as well as Cl distribution in plant tissue appear to be primarily governed by transpiration, since B and Cl in soil are highly mobile and move with water. Boron is supplied to roots primarily by mass flow. The factors affecting B uptake include soil type, B content, soil pH, amount of water soil receives, and plant species (Welch et al., 1991). Soil pH affects B absorption kinetics of roots, adsorption on soil particles, and maintenance of B concentrations in soil solution (Barber, 1995). The absorption of B by monocotyledonous plants was less than that by dicotyledonous plants and was passive (Shelp, 1993). Long-distance transport of B from roots to shoots occurs in the xylem and is related to the rates of transpiration (Brown and Shelp, 1997). Copper uptake is an active process (Dokiya et al., 1964) and is influenced by plant species, growth stage, plant part, various soil properties, and added amendments. Copper is relatively immobile in soil, so that large portions of Cu are derived from root interception in soils low in labile Cu (Oliver and Barber, 1966). The exploitation of soil by roots (root volume, density) influenced the Cu absorbed by roots (Barber, 1995). Soil pH did not affect Cu uptake extensively because the soil maintained sufficient levels of Cu, even when free Cu2+ had been reduced with increased soil pH (Barber 1995). Mycorrhizal associations with roots improved Cu uptake by 53 to 62% in white clover (Li et al., 1991).

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In soil solution, Fe3+ dominates and forms organic complexes with degraded OM (fulvic acid) or siderophores (Fe-complexing compounds released by soil microbes and/or plant roots) (Powell et al., 1982). In well-aerated soils, complexed Fe3+ is the major form of Fe. Higher plants use nonspecific and specific processes to increase the solubility and uptake of Fe from the rhizosphere. Uptake of cations over anions is one of the most important nonspecific processes that results in pH decreases in the rhizosphere to increase Fe availability and uptake (R¨omheld and Marschner, 1986). The factors that interfere with ionic balances in plants and contribute to Fe uptake are N source, K supply, plant P status, and genotypic differences (Zaharieva and R¨omheld, 1991). Strategy I processes used by dicotyledons and nongrass monocotyledons (nongraminaceous species) in responding to Fe deficiency are to excrete protons (acidification of rhizosphere) and increase reductase activity at the root–soil interphase. The iron deficiency in dicotyledonous plants is reduced by lowering the rhizosphere pH from the root H+ excretion (proton excretion), root exudation of organic acids (mainly phenolics), enhanced root reduction of Fe3+ to Fe2+, and activated root-reducing capacity at cell plasma membranes. Increased medium acidification and Fe3+ reduction are brought about by plasmalemma-linked H+: ATPase and NADH:Fe3+ reductase activities (Dell’Orto et al., 2000). Organic anions such as citrate and oxalate exudated from the roots contribute to the Fe mobilization in soil, and such a response appears to be the factors under P deficiency for species such as rape or lupin. (Hinsinger, 1998; Jones et al., 1996). In Strategy I plants, reduction activity at the root–soil interface appears to play a dominant role in Fe aquisiton (Bertrand and Hinsinger, 2000; Brown, 1978; Chaney et al., 1972). In Strategy I, plant response to Fe deficiency is the increased capacity of the roots to reduce ferric chelates (Bienfait, 1988), which is affected by HCO3−, Fe, and other metals (Alc´antara et al., 2000). Many monocotyledonous plants, especially those of Poaceae (grasses), transport Fe3+-phytosiderophores (root-derived chelates) across root cells (Strategy II plants), which is an important mechanism by which Fe is acquired by these plants. Strategy II processes are used by graminaceous species, which excrete several types of phytosiderophores as adaptive mechanisms to Fe deficiency (Kanazawa et al., 1993; Takagi et al., 1984). Phytosiderophores are low-molecular-weight polydentate (nonproteinogenic amino acids) ligands which bind Fe3+ to facilitate transport (Kochian, 1991; Marschner, 1995; R¨omheld, 1991; R¨omheld, and Marschner, 1986). Overall, the high pH, redox state, pH buffer (HCO3−, active lime, OM), nitrate, and Fe mineral types affect Fe uptake by plants (Lindsay, 1994; Lucena, 2000; Marschner, 1995; R¨omheld and Marschner, 1986). The rate of phytosiderophore release in cereals under Fe deficiency greatly differs between species, and these differences are positively correlated with the resistance of cereals to Fe deficiency (Marschner et al., 1986; R¨omheld and Marschner, 1990). ¨ urk, Besides Fe, phytosiderophores also mobilize Zn, Mn, and Cu (Cakmak, Ozt¨ et al., 1996; Hopkins et al., 1998; R¨omheld, 1991).

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Manganese uptake is metabolically mediated, and uptake increases from pH 4 to 6 (Maas et al., 1969). Above pH 6, oxidation of Mn2+ to Mn4+ occurs, and Mn2+ uptake is reduced. Soil pH and redox potentials control the Mn supply to roots by mass flow and diffusion. Deficiency of Mn usually occurs when soil pH is >6.2, but Mn2+ may be sufficient in some soils, even though the pH is ≥7.5 (Barber, 1995). The prevailing source of Mn at root surfaces is Mn2+. Manganese forms complexes with organic compounds (trihydroxamic acid, sideramines) of microbial and plant origin, which increases the Mn mobility in soil (Clarkson, 1988). The three major sources of Mn in soils that are primarily responsible for the Mn supply to roots are exchangeable Mn, organically complexed Mn, and Mn oxides (Marschner, 1988). The proportion of these Mn forms vary with soil type, soil pH, and OM. As the soil pH decreases, the proportion of exchangeable Mn increases dramatically, while the proportions of Mn oxides and Mn bound to Mn and Fe oxides decrease. In soils low in available Fe, root reductase activity is stimulated because of acidification of the rhizosphere and may lead to higher Mn mobility and uptake. Greater ranges in foliage Mn were noted for different species of plants growing in the same soil compared to Cu, Fe, or Zn (Gladstones and Loneragan, 1970). These differences were attributed to species ability to acidify soil in the rhizosphere rather than to the Mn requirement. Molybdenum is absorbed as an anion (MoO42−) and is energy dependent; S can interfere, and P enhances Mo uptake (Barber, 1995; Mengel and Kirkby, 1982). Mass flow and diffusion supply Mo to roots in soil (Table X). Zinc is absorbed primarily as a divalent cation (Zn2+) and may be absorbed at high soil pH as a monovalent cation (ZnOH+). It is not clear whether Zn uptake is active or passive, even though Mengel and Kirkby (1982) indicated that Zn was actively absorbed. Zinc is not reduced or oxidized as are Mn, Fe, and Cu. The low availability of Zn in high pH calcareous soils is due to the adsorption of Zn on clay or CaCO3 (Trehan and Sekhon, 1977). In addition, high concentrations of HCO3− inhibit Zn uptake and translocation (Dogar and van Hai, 1980). Zinc uptake is ¨ urk et al., 1996; Hopkins et al., also enhanced by phytosiderophores (Cakmak, Ozt¨ 1998).

C. OXIDATION AND REDUCTION Oxidation–reduction reactions occur when electrons are transferred from a donor to an acceptor. The donor loses electrons to increase in oxidation number, and the acceptor gains electrons to decrease in oxidation number. Redox reactions with various forms of Mn (Mn2+ and Mn4+), Fe (Fe2+ and Fe3+), and Cu (Cu+ and Cu2+) are common in soils (Lindsay, 1979), but Fe and Mn redox reactions are considerably more important than Cu because of their higher concentrations in soil. The primary source of electrons for biological redox reactions in soil is OM,

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217

but aeration, pH, and root and microbial activities also influence these reactions. Redox reactions in soil can also be influenced by organic metabolites produced by roots and microorganisms. Certain forms of micronutrients are more available to plants than others, and concentrations of each mineral form depend on soil conditions affecting redox. The most water-soluble and available forms to plants are Mn2+, Fe2+, and Cu2+, and these may be altered greatly depending on redox conditions. In general, a high pH favors oxidation and a low pH favors reduction of these minerals. The availability of Fe and Mn increases, and sometimes they become toxic to plants grown under highly reducing conditions (flooding). Redox of Mn is thermodynamically favored at relatively higher redox potentials compared to Fe at given pH values. For example, the critical redox potential at which Fe2+ appeared was 100 mV and Mn2+ appeared at 200 mV in a Crowley silt loam soil at pH 6.5 (Patrick and Jugsujinda, 1992). As a result, demonstrated spatial relationships between Mn and Fe precipitation in horizontal sand columns relative to increased redox potentials were observed (Collins and Buol, 1970). Iron precipitated at relatively lower redox potentials compared to Mn, which did not precipitate until reaching more oxidized portions in columns. Liming soil to pH > 5.6 increased oxidation processes and reduced or prevented Mn toxicity (Kamprath and Foy, 1985). Increased reduction of Mn oxides occurred with increased soil temperature (Ross and Bartlett, 1981; Sparrow and Uren, 1987). Hence, warm soils may induce Mn toxicity more readily than cooler soils. Flooding (reducing conditions) had no influence on B concentrations in soils, and B did not undergo redox reactions (Ponnamperuma, 1972). Increasing soil Eh values (oxidation) redistributed Cu from exchangeable and organic fractions to Fe oxide fractions, thereby reducing Cu availability to plants (Shuman, 1991). Under flooded conditions, Cu was adsorbed onto surfaces of reduced Mn and Fe oxides (Iu et al., 1981). Reducing conditions in soil mobilized Fe oxide fractions, which became associated with exchangeable, organic, and Mn oxide fractions to make Fe more available to plants (Shuman, 1991). Increases in Eh or soil pH shifted Fe from exchangeable and organic forms to water-soluble and Fe oxide fractions. Under alternate wetting and drying conditions, adding OM led to reducing conditions and enhanced Fe availability (Shuman, 1988). As redox potentials and/or soil pH increase, the plant availability of Fe decreases due to the insolubility of Fe3+ oxides. The critical redox potential for Fe3+ was −100 mV at pH 8, +100 mV at pH 7, and +300 mV at pH 6 (Gotoh and Patrick, 1974). Water-logging resulted in a decreased redox potential, and a low pH led to increased water-soluble and exchangeable Fe. Excess water in calcareous soil increased the buildup of HCO3−, which reduced soluble Fe3+ and induced Fe deficiency (Moraghan and Mascagni, 1991). Soil pH and redox potential are responsible for Mn transformation from insoluble to water-soluble and extractable forms. Under reducing conditions, Mn

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was released from organic and oxide forms into water-soluble and exchangeable fractions (Sims and Patrick, 1978). Low Eh values (reducing conditions) increased exchangeable Mn to mobilize Mn into more plant-available fractions (Shuman, 1991). In poorly drained soils, organic Mn and Mn oxides dominate compared to well-drained soils. Molybdenum does not appear to be directly involved in redox reactions in soil. However, the increases in soil pH and the reduction of Fe oxides under reducing conditions (low redox values) may increase the solubility of MoO4 (Moraghan and Mascagni, 1991). Zinc is not reduced under low redox conditions, but soil submergence tends to decrease Zn concentrations in soil solution (Ponnamperuma, 1972). Neither Zn nor Cu is affected by redox reactions which occur under most soil conditions. Submergence of soil caused Eh to decrease and pH to increase to enhance solubility and release oxide metals (Shuman, 1991). In flooded rice soils, decreased concentration and mobility of Zn was due to Zn adsorption on surfaces of hydrated Mn oxides (Singh and Bollu, 1983).

D. RHIZOSPHERE The rhizosphere is defined as the zone of soil immediately adjacent to plant roots in which the kinds, numbers, and/or activities of microorganisms differ from those of the bulk soil (SSSA, 1996). This zone usually contains fungi, bacteria, root and microorganism secretions, sloughed off or dead materials from microorganisms and roots, and chemical properties that are markedly different from the bulk soil. The chemistry of the rhizosphere has pronounced effects on the availability of micronutrients. An example of rhizosphere activity is mycorrhizae. Mycorrhizae associated with crop plants are primarily arbuscular mycorrhizal fungi (AMF). The AMF form beneficial symbioses with roots to allow plants to grow considerably better than would be expected under relatively harsh mineral stress conditions. These fungi are ubiquitous in most soils, and about 90% of plants are mycorrhizal. The AMF improve host plant nutrition by improving the acquisition of P and other minerals, especially the low mobile micronutrients Zn, Cu, and Fe (Marschner, 1991a). The AMF accomplish this primarily by extension of root geometry. That is, AMF hyphae are smaller (average diameter = 3–4 μm) than roots and/or root hairs (diameter = >10 μm) and can make contact with soil particles and/or explore pores/cavities that roots would not otherwise contact (Clark and Zeto, 2000). Hyphae also extend away from roots and explore greater volumes of soil than roots themselves. The AMF may also protect plants from excessive uptake of some toxic minerals (Brady and Weil, 1996; Clark and Zeto, 2000). Root colonization with

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AMF can decrease the risk of plants to Mn, Fe, B, and Al toxicity in acid soils (Clark and Zeto, 2000; Marschner, 1991a). Toxicity factors may be reduced by inhibiting the acquisition of toxic minerals and/or from root/hyphae exudations to decrease reactions in the rhizosphere like Mn reduction (Marschner, 1991a). In addition to mycorrhizae, noninfecting rhizosphere microorganisms may affect mineral nutrition of plants through their influence on growth and morphology of roots, physiology and development of roots and shoots, availability of nutrients, and nutrient acquisition (Marschner, 1995). Whether high microbial activity in the rhizosphere leads to increases or decreases in micronutrient availability depends on the conditions. For instance, if root exudates consist mainly of organic acids or complexing compounds with high activity toward mobilizing Mn or Fe, utilization of these organic acids by rhizosphere microorganisms may decrease the acquisition of Mn and Fe. The positive effects of rhizosphere microorganisms on micronutrient availability have generally been noted when sugars are released in root exudates (Marschner, 1991b). Noninfecting rhizosphere microorganisms may also be responsible for oxidation of Mn2+ in bulk and rhizosphere soils and may immobilize (oxidize) or mobilize (reduce) Mn (Marschner, 1995). Roots also induce chemical and microbial changes in the rhizosphere that affect micronutrient availability. The rhizosphere pH may differ by as many as 2–3 units from that bulk of soil (Marschner, 1995). The net excretion of H+,OH−, and HCO3− from roots associated with cation/anion uptake induces pH changes in the rhizosphere, which have been related to soil buffer capacity and source of N. Root excretion of H+ at root surfaces is an effective mechanism for enhancing Zn uptake compared to excretion of complexing agents (Bar-Yosef et al., 1980). Acidification of the rhizosphere generally improves availability of micronutrients, even in calcareous soils, to enhance micronutrient mobilization. This has been noted especially for Fe. Enhanced reducing activity at root surfaces has been noted as root-induced responses to Fe deficiency in dicotyledonous and nongraminaceous monocotyledonous plants (Marschner, 1995). Modification of rhizosphere properties by roots is important in micronutrient acquisition by plants and plant ability to adapt to adverse mineral stress soil conditions (Marschner, 1995). Plant roots release or secrete low- and high-molecular-weight root exudates. Low-molecular-weight exudates include organic, amino, and phenolic acids (including phytosiderophores) and sugars. These low-molecular-weight exudates released from roots mobilize micronutrients in the rhizosphere and assist roots in acquiring less available minerals. The effectiveness with which root exudates dissolve sparingly soluble micronutrients depends on rhizosphere pH, N form, mineral deficiency-induced H+ excretion, and/or microbial acid production (Marschner, 1988). The major components of high-molecular-weight substances released to the rhizosphere are mucilages and ectoenzymes. These substances contribute to

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rhizodeposition (deposition of organic C). High-molecular-weight organic C exudates released into the rhizosphere serve as substrates for microorganisms around roots and may indirectly affect the solubility and availability of micronutrients (Curl and Truelove, 1986; Marschner, 1995). Microorganisms in the rhizosphere can benefit plant growth by enhancing nutrient availability (mineralization, root morphology, fauna activity), increasing nonsymbiotic N2 fixation, improving symbiotic root relationships with other microorganisms (rhizobia, mycorrhizae), enhancing plant responses to microbial metabolites, and decreasing plant pathogen activity and diseases (Curl and Truelove, 1986). Considerable amounts of C may be released by plants into the rhizosphere. On average, 30–60% of the net photosynthetic C is allocated to roots, and appreciable proportions of this C (14 to 40% of fixed C) are released as organic C into the rhizosphere (Marschner, 1995). The amount of C released depends on plant age and growing conditions such as plant water status, soil aeration, soil strength, and nutritional status of plants (Whipps and Lynch, 1986). Rhizosphere deposition of organic C normally increases when various forms of stress such as mechanical impedance, anaerobiosis, drought, and mineral deficiencies occur (Lynch and Whipps, 1990; Whipps and Lynch, 1986). Soil microbes mineralize SOM, thereby releasing large amounts of essential mineral nutrients. Microorganisms at root surfaces may also affect root morphology (main root and root hair density, surface area), and subsequently enhance or reduce mineral absorption (Curl and Truelove, 1986). The release of root exudates increased soluble Cu concentrations (Nielson, 1976), and the dissociation of Cu2+ from organic ligands occurred prior to plant uptake (Goodman and Linehan, 1979). Reducing processes near roots can increase available Fe3+ from dissociation of Fe3+–chelates (R¨omheld and Marschner, 1986). Organic acids may also be responsible for the mobilization of sparingly soluble Fe (Fe3+) in the rhizosphere. Plant responses to Fe deficiency may increase the exudation of phenolic and amino acids, especially phytosiderophores, so that plants may acquire Fe (Marschner, 1995). Root exudation from Fe-deficient barley grown in calcareous soil mobilized considerable amounts of Fe, Zn, Mn, and Cu (Treeby et al., 1989). Organic compounds such as hydroxy-carboxylates released from roots enhanced the Mn availability by reducing Mn4+ oxides and complexing Mn2+ (Godo and Reisenauer, 1980). Such effects of root exudates are particularly important in soils at pH < 5.5. Acquisition of Mn by rice grown in aerobic soil apparently was influenced by Fe uptake and soil pH (Jugsujinda and Patrick, 1977). Increased solubility of MnO2 by root exudates resulted mainly from organic acids (Uren and Reisenauer, 1988). For example, exuded organic, amino, and phenolic acids may directly enhance dissolution of sparingly soluble Mn compounds in soil. The effectiveness of root exudates for dissolution (reduction) of Mn oxides is favored at low and inhibited at high rhizosphere pH.

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E. INTERACTIONS WITH OTHER ELEMENTS The understanding of micronutrient interactions between and among the various mineral nutrients is important for balancing nutrient supplies to plants, improving growth and yields of plants, and eliminating deficiencies and toxicities imposed on plants. Mineral interactions are generally measured in terms of growth responses and changes in mineral nutrient concentrations in plants. An excellent review of the many interactions micronutrients have with other elements has been provided by Olsen (1972), and our article discusses mostly information since that review.

1. Boron The ability of anions to leach adsorbed B from Fe and Al oxides in soil increased in the order of Cl < S  P (Metwally et al., 1974). Magnesium hydroxides also adsorb B (Rhoades et al., 1970). Normal B concentrations in plant tissue usually range from 10 to 50 mg kg−1 dry wt, but some plants like alfalfa require considerably more than others (Mengel and Kirkby, 1982). Positive relations have also been noted between B and K and N fertilizers for improving crop yields (Hill and Morrill, 1975; Moraghan and Mascagni, 1991). High B supplies resulted in low uptake of Zn, Fe, and Mn, but increased uptake of Cu. High pH, Ca, Mg, and N in soil may also reduce B in plants. In low B soil, high N induced B deficiency in plants (Gupta, 1993). However, the effects of P, K, and S on uptake of B are not clear, and these minerals had positive, negative, and/or no effects on B uptake (Gupta, 1993). Zinc deficiency enhanced B accumulation (Graham et al., 1987), and Zn fertilization reduced B accumulation and toxicity on plants grown in soils containing adequate B (Graham et al., 1987; Moraghan and Mascagni, 1991; Swietlik, 1995). Boron deficiency reduced uptake of P by faba bean (Robertson and Loughman, 1974) and reduced uptake of Mn and Zn by cotton (Ohki, 1975). Boron became toxic to maize when grown under P deficiency conditions, and P applications alleviated B toxicity (G¨unes and Alpaslan, 2000). Calcium translocation to shoots was inhibited because of the relatively high xylem sap pH, which was improved by applying B (Singaram and Prabha, 1997). Root Ca concentrations decreased while B concentrations increased, but B in shoots and fruit did not change, indicating that B translocation was not hindered by Ca in plants grown in calcareous soil. On the basis of equivalent Ca/B ratios, both foliar and soil applications of B insured adequate B to shoots and alleviated excess Ca uptake from soil (Moraghan and Mascagni, 1991). Even though the role of B in plants is not clearly understood, B is important in membrane structure, transport across membranes, metabolism of cellular N and P compounds, and viability of seeds (Kastori et al., 1995; Rerkasem et al., 1997). These processes

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would indirectly affect uptake of not only B but also other minerals. Uptake and transport of various mineral nutrients in plants are sensitive to B concentrations in the growth media (Mozafar, 1989). 2. Chlorine Only limited information is available on interactions of Cl with other nutrients. Chlorine is highly mobile in soil, and excessive concentrations can be leached by excess irrigation and/or rainfall. High concentrations of Cl in soil solution may depress mineral nutrient activities and produce abnormal Na/Ca, Na/K, Ca/Mg, and Cl/NO3–N ratios. As a result, plants may become susceptible to osmotic injury as well as nutritional disorders that could reduce plant yield and quality (Grattan and Grieve, 1999). Chloride is often added with K fertilizers, which are added at relatively high rates compared to other micronutrients. Increased levels of Cl reduced NO3–N (Inal et al., 1995) as Cl competes with NO3–N during uptake processes (Mengel and Kirkby, 1982). Evidence exists that if Cl rather than SO4–S is dominant in saline soils, Ca deficiency can be alleviated, and Cl may increase Ca uptake independent of Ca addition (Curtin et al., 1993). Chloride enhancement of Ca may also be related to increases in cation activity from Cl in soil solution or from co-transport resulting in neutralization of positive charges during cation uptake (Marschner, 1995). Ranges of Cl concentrations normal for tissue are high even though amounts needed for plant activity are relatively low (Mengel and Kirkby, 1982). 3. Copper Copper uptake is metabolically mediated and strongly inhibited by other divalent cations, especially Zn2+ (Mengel and Kirkby, 1982). Applications of relatively high levels of N and P fertilizers have induced Cu deficiency on plants grown in low Cu soils. Even though N and Cu interact, no significant effects of NO3–N or NH4–N on Cu uptake have been noted (Kochian, 1991). However, transport of Cu was related to supply and transport of N, and Cu translocation increased with increasing N supplies (Jarvis, 1981b). Increased soil P induced Cu deficiency, but was related to dilution effects from increased growth and depressing effects of P on Cu absorption (Reuter et al., 1981). Copper toxicity has also been noted in P-deficient plants (Wallace, 1984), and K also decreased Cu uptake in sunflower (Graham, 1979). Plants grown in coarse-textured soils with low available P and Fe and high in Cu exhibited Cu toxicity (Moraghan and Mascagni, 1991). Added Fe ameliorated Cu toxicity in spinach (Ouzounidou et al., 1998), and Cu toxicity has induced Fe deficiency in plants (Bowen, 1969). Increased Cu in the growth media, decreased Zn, and increased P levels in soil resulted in a reduced exploration of soil by mycorrhizal roots, which led to low Cu availability and low Cu concentrations

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in plant tissue (Moraghan and Mascagni, 1991). Since Zn and Cu are absorbed by the same carrier, each of these mineral nutrients competitively inhibits uptake of each other (Giordano et al., 1974). Microbial immobilization and antagonistic effects of increased concentrations of Fe and Mn reduced soil-available Cu. 4. Iron High soil levels of several minerals (Ca, P, N, Mn, and Cu) may contribute to the induction of Fe deficiency in many plants (Madero et al., 1993). On the other hand, low soil Fe may also inhibit or promote absorption of other minerals. Of the nutrients that interfere with Fe nutrition, minerals with the greatest effects followed the sequence of P > K > Mg > N > Ca (Luo et al., 1997). High Fe may also reduce uptake of these minerals. Different concentrations of Fe inhibited mineral uptake by rice grown in nutrient solution and uptake of P, K, Ca, Mg, and S by alfalfa, wheat, rice, and red clover also decreased with increased levels of Fe (Fageria, Baligar, and Edwards, 1990; Fageria and Rabelo, 1987). Similarly, uptake of Mn, Zn, and Cu in alfalfa, red clover, and wheat decreased when Fe concentrations increased. Increasing Cu in the growth medium decreased not only Fe but also Zn and Mn (Alva and Chen, 1995). However, the effect on Fe was more pronounced than that on Zn and Mn. Negative interactions between Fe and Mn have also been reported for other crop plants (Moraghan, 1985; Zaharieva, 1986). Soils low in Zn may enhance Fe uptake, especially when soil pH is >7.0 (Fageria and Gheyi, 1999). The effects of high soil P on decreasing plant Fe concentrations because of immobilization of soil Fe are well documented (Olsen, 1972), and high soil P levels decreasing plant Fe concentrations may also be related to inhibition of Fe absorption by roots, subsequent transport to shoots, and inactivation of Fe in plants (Moraghan and Mascagni, 1991). Nitrogen, especially NO3–N, can aggravate Fe deficiency by raising soil pH (Aktas and Van Egmond, 1979; Wallace et al., 1976) and release of HCO3− in the rhizosphere (Chen and Barak, 1982). With or without N fertilizer, the application of Fe resulted in increased N, P, K, Mg, Zn, and Cu concentrations in leaf blades of peanut, but decreased Ca and Mn (Ali et al., 1998). Manganese decreased Fe uptake and adversely affected Fe metabolism (Zaharieva et al., 1988) and increased Mo-decreased Fe uptake (Olsen and Watanabe, 1979). This latter interaction may be important in alkaline soils where Fe availability is low and soluble MoO42− concentrations may be high. Iron toxicity is common for rice grown in flooded soils because of enhanced reducing conditions (Fe3+ to Fe2+), and Fe concentrations in solution and plants increase (Fageria, Baligar, and Wright, 1990). The nutritional status of rice is commonly related to Fe toxicity. When Fe toxicity occurs in rice, Fe concentrations in leaf blades may exceed 300 mg kg−1 dry wt (Fageria, Baligar, and Wright, 1990; Yoshida, 1981). In addition, P, K, Ca, Mg, and Mn deficiencies decrease the capacity of rice roots to exclude Fe, and Fe toxicity may result. In soils where

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problems of Fe toxicity exist, P and K deficiencies appeared before uptake of Mn, Zn, and Cu was reduced. Adequate concentrations of K in soil solution also decreased Fe toxicity in rice (Fageria, Baligar, and Edwards, 1990). Zinc deficiency may accentuate Fe uptake and lead to the accumulation of toxic levels of Fe in plants (Adams and Pearson, 1967).The addition of MnO2 increased soil redox potential and reduced concentrations of Fe2+ and organic reducing products (Fageria, Baligar, and Wright, 1990). Iron toxicity is more severe for plants grown on heavy-textured soils compared to light-textured soils. 5. Manganese The anionic minerals P, S, NO3–N, and Cl and the cationic minerals K and NH4–N affect solubility, mobility, and/or availability of Mn to crop plants (Norvell, 1988). Studies on the interactions between Mn and divalent minerals are also common (Bowen, 1969; Chinnery and Harding, 1980). Manganese uptake is considered to be active and may be inhibited by Ca, Mg, and Zn (Maas et al., 1969; Robson and Loneragan, 1970). Relatively high concentrations of Fe were noted in leaves of soybean grown with low Mn, and Mn concentrations in soybean shoots decreased with increased Fe levels in solution (Chinnery and Harding, 1980). Free CaCO3, high Fe, and strongly alkaline conditions may also induce Mn deficiency in plants. The application of Fe may reduce concentrations of Mn in plants. Plants grown with Fe applications had high plant growth and low shoot Mn concentrations, even to deficiency levels, because of dilution (Romero, 1988). The antagonistic effects of FeEDDHA on Mn accumulation were reported in white lupin, but these effects occurred mainly when relatively high amounts of P were added (Moraghan, 1992). Relatively low levels of Fe (4 mg kg−1 soil) in the absence of added P had only slight negative effects on Mn and even increased Mn concentrations. In contrast, marked depressing effects of FeEDDHA on Mn concentrations were noted for plants grown with high P (120 mg kg−1 soil). Problems associated with Fe–Mn interactions have been related mainly to chemical interactions at the root–soil interface (Kochian, 1991). Increased rhizosphere acidity from plant responses to Fe deficiency may also enhance Mn4+ reduction to Mn2+, and increase Mn2+ solubility (Marschner, 1988). Increased levels of soil P both increased and decreased Mn toxicity in plants, and applications of Zn or Mo fertilization reduced Mn uptake (Moraghan and Mascagni, 1991). Increasing concentrations of Fe (also Ca or Mg) in the growth medium may also decrease Mn toxicity (Marschner, 1995). Excess Mn-induced Fe deficiency in potato and leaves had Mn/Fe ratios of 18 or higher (Lee, 1972). The high Al availability counteracted these effects by increasing Fe in plants and decreasing Mn/Fe ratios. Plants with Fe deficiency had lower Mn/Fe ratios, and plants with higher ratios developed Mn toxicity (Lee, 1972). Manganese toxicity and Fe deficiency symptoms are different in rice, and the range at which Fe toxicity can be remedied by Mn application is narrow (Tanaka

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and Navasero, 1966). High shoot Fe concentrations of Fe-inefficient, Mn-sensitive soybean accentuated Mn toxicity, and high shoot K concentrations of Mn-tolerant soybean alleviated the harmful effects of high internal Mn concentrations (Brown and Jones, 1977). The increased Ca levels in the growth medium decreased Mn uptake and toxicity (Heenan and Carter, 1976). Phosphorus detoxified Mn by precipitating it within plant roots (Heintze, 1968). Soluble sources of Si in the growth medium can also protect plants against Mn toxicity (Foy et al., 1978). Plants low in Si, P, Ca, Mg, and Fe often accumulate high Mn and are susceptible to Mn toxicity (El-Jaoual and Cox, 1998). Silicon may also decrease excessive uptake of Mn and Fe (Foy et al., 1978). Excess Mn can interfere with absorption, translocation, and utilization of P, Ca, Mg, and Fe (Clark, 1982) and reduce concentrations of Si, K, Zn, and Cu (Clark and Baligar, 2000). Increasing Mn concentrations in nutrient solution triggered synergistic effects on Ca, Mg, Na, P, and Cu uptake, but displayed antagonistic action on K and Zn in rice (Lidon, 1999). Translocation of Fe was also inhibited. Increasing Mn levels delayed rice maturation and the concentrations of the minerals accumulated. However, concentrations of potentially toxic minerals in grain were lower than those in vegetative tissues. Concentrations of Ca, K, Na, P, and Zn interacted with increasing Mn concentrations, mostly in shoots, but different patterns were noted for Mg, Cu, and Fe. Manganese acquisition was reduced with the application of Zn (Haldar and Mandal, 1981) and Mo fertilizers (Sims et al., 1975). Interactions of Mn with other elements, particularly Fe and Si, may be extensive (El-Jaoual and Cox, 1998). 6. Molybdenum Sulfur, P, and NH4–N applications may decrease Mo concentrations in plants and accentuate Mo deficiency (Anderson, 1956; Gupta and MacLeod, 1975; Ray et al., 1986). Soil application of Mo increased Mo and N uptake by legumes at soil pH 5 (Mortvedt, 1981). High Fe and Al oxides and good soil aeration (drainage) also reduced Mo availability. Sulfur has been used to decrease Mo uptake and reduce Mo toxicity in plants through decreasing soil pH (Chatterjee et al., 1992). Increased B and decreased K, Mn, and Cu were noted in barley grown with high Mo (Brune and Dietz, 1995). High Mo may also induce Cu deficiency in cattle (“molybdenosis”) (Miller et al., 1991). Although Mo is essential to higher plants, its concentration in tissue is low (usually < 1 mg kg−1 dry wt) and crucial in N metabolizing enzymes (nitrate reductase) (Beevers and Hageman, 1969; Yu et al., 1999). 7. Zinc Zinc interactions with other elements are many and include Zn–P, Zn–N, Zn–K, Zn–Mn, Zn–Fe, and Zn–Cu (Moraghan and Mascagni, 1991; Olsen, 1972). Under

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some conditions, Co and Na may also inhibit Zn absorption (Loneragan and Webb, 1993). The most widely reported interaction with Zn is that of P. High P applied to low Zn soils enhanced the plant accumulation of P thereby increasing the internal plant Zn requirement because of Zn precipitation (Robson and Pitman, 1983). High applications of P fertilizer can induce Zn deficiency (P-induced Zn deficiency) and increase plant requirements for Zn (Robson and Pitman, 1983). Inappropriately high P applications have induced Zn deficiency in plants most likely because of increased P uptake and higher shoot growth, which has led to decreased Zn in shoots because of dilution (Loneragan et al., 1979; Marschner, 1993). Zinc-deficient plants may also have high and potentially toxic P concentrations, and P toxicity symptoms have sometimes been mistaken for Zn deficiency (Fageria and Gheyi, 1999). Nevertheless, Zn-deficiency-induced P toxicity may be an artifact caused by high P concentrations (Loneragan and Webb, 1993). High levels of P have also resulted in increased absorption and retention of Zn in roots and decreased translocation to leaves (Iorio et al., 1996). The processes involved with P–Zn interactions and the subsequent low acquisition of Zn by plants include high P in soil decreasing Zn solubility, reduced root growth, cations added with and H+ generated by P salts to inhibit Zn absorption, and suppressed root colonization by mycorrhizae (Loneragan and Webb, 1993; Robson and Pitman, 1983). Plants with reduced mycorrhizal root colonization had lower Zn concentrations (Lambert et al., 1979), and mycorrhizal plants commonly have higher Zn concentrations than nonmycorrhizal plants (Clark and Zeto, 2000). In certain soils, added P tended to enhance the adsorption of Zn on soil particles rich in hydrated Fe and Al oxides with subsequent inducement of Zn deficiency on plants (Barber, 1995). Many interactions of Zn with macronutrients other than P have been noted. Both monovalent and divalent cations can inhibit Zn uptake, and the importance of these were NH4–N > Rb > K > Cs > Na > Li for monovalent minerals and Mg > Ba > Sr = Ca for divalent minerals (Chaudhry and Loneragan, 1972a,b). The application of gypsum to sodic soils and the addition of manures have also helped alleviate Zn deficiency (Takkar and Walker, 1993). Alkaline soils and soils high in CaCO3, N, and P and low in SOM normally have reduced Zn availability. High levels of H+ also competitively reduced Zn absorption (Barber, 1995). With increased supplies of S, increased Zn was translocated from roots to shoots (Fontes and Cox, 1998a). High levels of Zn decreased uptake of Cu and Mn in upland rice grown in an Oxisols in central Brazil. Zinc interactions with other micronutrients include enhanced B concentrations in Zn-deficient plants (Singh et al., 1990) and B toxicity being reduced with Zn applications (Graham et al., 1987; Singh et al., 1990). Mutually competitive interactions occur between Cu and Zn (Barber, 1995; Loneragan and Webb, 1993). Zinc–Cu interactions affected plant nutrition because Zn strongly depressed Cu absorption, Zn and Cu competitively inhibited each other, and Cu affected

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redistribution of Zn within plants (Loneragan and Webb, 1993). Enhanced Zn supplies improved the growth of Fe-deficient soybean (Fontes and Cox, 1998a), and Fe applications overcame many soybean Zn toxicity effects (Fontes and Cox, 1998b). Increased soil Zn increased translocation of Mn to soybean shoots to induce Mn toxicity (crinkle leaf), and Zn and Mn interfered with Fe utilization in leaves to reduce chlorophyll synthesis (Foy et al., 1978) . In addition, Zn deficiency enhanced uptake of Mn so that Mn concentrations reached phytotoxic levels (Robson and Pitman, 1983). Increased concentrations of Mn, B, and Mo were also noted when barley received Zn applications (Brune and Dietz, 1995). 8. Nickel and Cobalt Maize grown in calcareous soil with Ni applications enhanced Zn and decreased P concentrations (Karimian, 1995), and high levels of Ni increased B, Mn, and Mo in barley (Brune and Dietz, 1995). Simultaneous supplies of NO3–N and NH4–N reduced Ni toxicity in sunflower, and growth was enhanced from added Ni (Zornoza et al., 1999). Low Ni plants became N deficient from lack of urease activity with a high accumulation of urea but low tissue N (Gerendas and Sattelmacher, 1997). Cobalt availability was decreased in soils containing high CaCO3 and high Fe, Mn, SOM, and moisture. Added Co to growth media increased N, P, Ca, and Cu, but had no enhancement effects on K, Mg, Na, and Zn in tomato (Moreno-Caselles et al., 1997). Calcium and Mg noncompetitively inhibited Ni uptake, whereas Cu, Zn, and Co competitively inhibited Ni absorption (Korner et al., 1987).

V. IMPROVING SUPPLY AND ACQUISITION A. SOIL IMPROVEMENT Production potentials of many soils in the world are decreased by low supplies of micronutrients from adverse soil physical and chemical constraints (Baligar and Duncan, 1990; Baligar and Fageria, 1997; Dudal, 1976; Fageria, 1992; Fageria and Baligar, 1997a; Fageria, Baligar, and Edwards, 1997; Fageria, Baligar, and Wright, 1997; Foy, 1984). Major chemical (salinity, acidity, elemental deficiencies and toxicities, low SOM) and physical (bulk density, hardpan layers, structure and texture, surface sealing and crusting, water holding capacity, water-logging, drying, aeration) constraints affect transformation (mineralization, immobilization), fixation (adsorption, precipitation), and leaching or surface runoff of indigenous and added micronutrients (Baligar and Bennett, 1986a,b; Baligar and Fageria, 1997). In tropical regions, common soil micronutrient problems in rainfed systems affecting crop production include Fe toxicity and Zn deficiency (Baligar and

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Fageria, 1997; Fischer, 1998). Acid soils present special micronutrient nutritional problems for plants because of the high availability of Mn and Fe and the reduced availability of Zn and Mo (Baligar and Fageria, 1997; Fageria, Baligar, and Edwards, 1990; Fageria, Baligar, and Wright, 1990; Sumner et al., 1991). In addition, factors enhancing acidification not only lead to micronutrient toxicities/deficiencies but also to soil degradation (Baligar and Ahlrichs, 1998; Baligar et al., 1998; Dudal, 1976; Sumner et al., 1991). Micronutrients commonly occurring in toxic concentrations in salt-affected soils-include Mo and B (Gupta and Abrol, 1990). In recent years, the addition of toxic trace elements like Cd, Cr, Ni, Pb, Cu, Zn, As, Co, and Mn (some of which are considered micronutrients) to agricultural soils has increased from enhanced anthropogenic activity (burning fossil fuels, application of sewage, industrial, mine, municipal products), use of amendments (fertilizers, manures, lime), application of pesticides, and deposition of atmospheric particles (Adriano, 1986; Alloway, 1995a,b; Kabata-Pendias and Pendias, 1992). Excessive levels of trace elements pose phytotoxicities to plants and may reduce growth and acquisition of micronutrients (Baligar et al., 1998; KabataPendias and Pendias, 1992; Marschner, 1995). Temperature, pH, redox potentials, anion ligand formation, and composition and quantity of solution greatly influence the mobility and bioavailability of micronutrients and other trace elements in soil (Alloway, 1995b). The bioavailability of most trace elements is high at low soil pH. Adverse soil physical properties affect longitudinal and radial root growth, root distribution, morphological (stunting, thickening, reduction of lateral roots) and anatomical changes (Bennie, 1996; Russell, 1977; Taylor et al., 1972). High mechanical impedance leads to the loss of root caps and the reduction of root thickening, primarily due to short and wide cells of the same cortex volume (Camp and Lund, 1964) and thick cortex cells (Baligar et al., 1975). Mechanical impedance may also cause changes in the structure of the endodermis and pericycle cells (Baligar et al., 1975; Bennie, 1996). Such changes in root size and internal and external morphology will influence root ability to explore large soil volumes for micronutrients. Excessive or deficient micronutrients also affect morphology (length, thickness, surface areas, density) and growth (dry mass, root : shoot ratio) of roots and root hairs (Baligar et al., 1998; Bennett, 1993; Hagemeyer and Breckle, 1996; Fageria, Baligar, and Jones, 1997; Fageria, Baligar, and Wright, 1997; Foy, 1992; Kafkafi and Bernstein, 1996; Marschner, 1995). Maize root : shoot ratios increased when Zn was decreased and decreased when Mn and Cu were decreased (Clark, 1970). Organic matter helps maintain good soil aggregation, increases water holding capacity and exchangeable ions, leaching of nutrients, and Mn and Fe toxicities (Baligar and Fageria, 1997; Fageria, 1992; von Uexkull, 1986). The addition of crop residues, green manures, composts, animal manures, growing cover crops,

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using reduced tillage, and avoiding elimination (burning) of crop residues can significantly improve SOM levels and eventually lead to improved plant growth and acquisition of micronutrients. Liming has also been effective in correcting soil chemical constraints (Adams, 1984) and has improved the availability of Mo and decreased the availability of Mn, Fe, B, Zn, and Cu, and reduced Mn toxicity (von Uexkull, 1986). Liming also improves root growth to increase plant ability to absorb micronutrients. In addition, liming improves soil capacity to supply needed micronutrients to plants (Baligar and Fageria, 1997; Fageria, 1992; Fageria et al., 1995).Since lime has low mobility in soil, surface-applied lime has little or no effect on improving problems in subsurface soil. However, the tendency for downward movement of Ca from surface-applied gypsum (CaSO4) is high (Farina and Channon, 1988; Farina et al., 2000; Ritchey et al., 1980, 2000) and has long-term positive effects on plant growth (Farina et al., 2000; Toma et al., 1999). The downward movement of Ca in soil improved the rooting depth and increased the levels of micronutrients for maize grown in Cerrado acid soils of Brazil (Sousa et al., 1992). The reduction of subsoil acidity problems usually leads to deeper rooting and improves micronutrient uptake by plants.

B. SOIL AND FOLIAR FERTILIZATION The sources of micronutrients may be inorganic, synthetic chelates, and/or natural organic complexes. The potential exists for creating toxic levels of micronutrient in soil by misapplication, since only small amounts are leached from soil (except B) or small quantities are absorbed by plants (Martens and Westermann, 1991). Micronutrient toxicities are undesirable as they lower yields and product quality, and excessive levels may enter the food chain. The remediation of soils with high levels of micronutrients is relatively difficult. The factors influencing availability and plant acquisition of micronutrients have been discussed in earlier sections. Both organic and inorganic micronutrient sources are used to correct deficiencies in soil. Soil application includes band or broadcast applications before planting or foliar sprays during vegetative growth. Micronutrients are usually blended with or coated onto granular N, P, and K fertilizers or mixed with fluid fertilizers (Mortvedt, 1991, 2000). To prevent chemical alteration of micronutrients, blending should occur relatively soon before application (Mortvedt, 1991). Foliar applications are used to supply micronutrients more rapidly for correction of severe deficiencies commonly induced during the early stages of growth, and are temporary solutions to the problem. Several problems associated with foliar applications include low penetration rates in thick leaves, run-off from hydrophobic surfaces or being washed off by rain, rapid drying of spray solution, limited

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translocation from uptake site to other plant parts, limited amounts of nutrients that can be supplied and often do not meet plant demands, and leaf damage/burn (Marschner, 1995). Reducing the pH of spray solutions may reduce leaf damage. The addition of Si-based surfactants appears to reduce leaf damage and increase spray effectiveness (Horesh and Leavy, 1981). The disadvantages of foliar application are maximum yields which may not be possible if spraying is delayed until deficiency symptoms appear and residual effects from foliar sprays are little, thus multiple sprays may be required for season-long correction (Mortvedt, 2000). However, foliar fertilization has many advantages which include: rates applied are considerably lower than soil applications; uniform applications are possible; crop response to applied micronutrient is almost immediate so that deficiency can be corrected relatively rapidly; problems often associated with inactivation of soil-applied micronutrients may be overcome (Mortvedt, 2000). Plant (leaf age, species, nutritional status and requirements), climatic (light, temperature, humidity), and chemical (form, carrier, adjuvant) factors affect foliar spray effectiveness (Kannan, 1990). Greater absorption by leaves is favored under low light, optimum temperature, and high humidity conditions. Young leaves are metabolically more active than older leaves and are more effective with absorption. Hygroscopic compounds keep micronutrients in solution longer, thereby helping plants absorb these elements more effectively than nonhygroscopic compounds. To increase the effectiveness of foliar uptake, wetting agents are usually added to sprays. These chemicals are neutral nonionic compounds which reduce surface tension and increase wetting of leaf surfaces to enable larger amounts of solution to be absorbed (Kannan, 1990). 1. Correcting Deficiencies The measures for correcting micronutrients are summarized in Table XI. This information includes concentrations of nutrients for soil and foliar spray applications. The concentrations listed are approximate and may vary depending on original soil level, crop species/cultivar, crop yield desired, and climatic conditions. Issues related to soil and foliar fertilization of micronutrients and correcting their deficiencies in soil and plants have been discussed (Martens and Westermann, 1991; Mortvedt, 1991, 2000). Crop recovery of micronutrients is relatively low (5 to 10%) compared to that of macronutrients (10 to 50%) because of poor distribution from low rates applied, fertilizer reactions with soil to form unavailable products, and low mobility in soil (Mortvedt, 1994). The principal sources of micronutrient fertilizers used have been listed in Table XII. Boron is usually applied at 0.25 to 3 kg ha−1, and higher rates are required for broadcast than for band application or foliar sprays (Mortvedt and Woodruff, 1993). Legumes and certain root crops require 2 to 4 kg B ha−1, while lower rates are usually necessary for maximum yields of other crops (Martens and Westermann,

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Table XI Methods of Correcting Micronutrient Deficienciesa Corrective measure Element B Cl Cu

Soil applicationb 0.25–7 kg borax ha−1 (soil application preferred) 20–50 kg KCl ha−1 1–20 kg CuSO4 ha−1 (every 5–10 years)

Zn

30–100 kg FeSO4 or FeEDDHA ha−1 (need annual treatment of 0.5–10 kg ha−1) 5–50 kg Mn source ha−1 (soil application not recommended) 0.01–1 kg Mo source ha−1 (0.3 Na or NH4 molybdate ha−1) or lime to pH 6.5 0.5–35 kg ZnSO4 or ZnEDTA ha−1

Ni Co

Usually not needed 1–6 kg Co source ha−1 (broadcast)

Fe

Mn Mo

Foliar applicationc 0.1–0.25% B solution or 1–10 kg B ha−1 Unknown 0.1–0.2% solution CuSO4·5H2O or 0.1–4.0 kg Cu ha−1 as CuCl2·2H2O, CuSO4·5H2O, or CuO 2% FeSO4·7H2O or 0.02–0.05% FeEDTA solution (several sprays needed) 0.1% MnSO4·H2O solution or 0.3–6 kg Mn ha−1 0.07–0.1% Na or NH4 molybdate (100 g Mo ha−1) 0.1–0.5% ZnSO4·7H2O solution (0.17–1.5 kg ha−1) May be applied as spray 500 mg Co L−1 solution or 500 mg Co kg−1 seed treatment

a From Bould et al. (1983), Fageria, Baligar, and Jones (1997), and Martens and Westermann (1991). b Lower values for soil applications are applicable for band application and higher values are for broadcast applications. c 400 liters of solution is sufficient to spray 1 ha of field crop.

1991). Using the concept of Ca/B ratios, the application of foliar (0.3%) or soil (10 kg ha−1) B ensured adequate B (Moraghan and Mascagni, 1991). Borax or other soluble borates are usually applied to soil before planting. Boron fertilizer should not be placed in contact with seeds or at levels that may be toxic to crops. Boron availability commonly decreases during drought and when acid soils are limed (Martens and Westermann, 1991). Even though Cl has been recognized as essential to plants, comparatively little attention has been given to Cl as a fertilizer because soil levels from inputs and rain are considered adequate to meet crop requirements. Chlorine may become limiting for high yields in intensive production practices. Positive yield responses were noted for application of 400 kg Cl ha−1 for maize (Heckman, 1995). Winter wheat yields were also increased with Cl applications at seven of nine experimental sites (Engel et al., 1994). Only a few land areas are deficient in Cl, and crops grown

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FAGERIA et al. Table XII Principal Sources of Micronutrient Fertilizers to Correct Deficienciesa

Element B

Cl

Cu

Fe

Mn

Mo

Zn

Source

Formula

Boric acid Borax Na borate (anhydrous) Na pentaborate Na tetraborate Boron frits K chloride Zn chloride Ca chloride Mn chloride

H3BO3 [B(OH)3] Na2B4O7·10H2O Na2B4O7 Na2B10O16·10H2O Na2B4O7·5H2O Fritted glass KCl ZnCl2 CaCl2 MnCl2

Cu sulfate (monohydrate) Cu sulfate (pentahydrate) Cu chloride Cuprous oxide Cupric oxide Cu chelate Cu chelate Ferrous sulfate (monohydrate) Ferrous sulfate (heptahydrate) Ferrous ammonium sulfate Ferric sulfate Fe chelate Fe chelate Fe chelate Fe chelate Fe frits Mn sulfate (anhydrous) Mn sulfate (tetrahydrate) Mn chloride Mn carbonate Mn oxide Mn chelate Mn frits Na molybdate Ammonium molybdate Mo trioxide Molybdic acid Mo frits Zn sulfate (monohydrate) Zn sulfate (heptahydrate) Zn chloride Zn oxide Basic Zn sulfate

CuSO4·H2O CuSO4·5H2O CuCl2 Cu2O CuO Na2CuEDTA NaCuHEDTA FeSO4·H2O FeSO4·7H2O (NH4)2SO4·FeSO4·6H2O Fe2(SO4)3·4H2O NaFeEDTA NaFEHEDTA NaFeEDDHA NaFEDTPA Fritted glass MnSO4 MnSO4·4H2O MnCl2 MnCO3 MnO Na2MnEDTA Fritted glass Na2MoO24·2H2O (NH4)6Mo7O24·4H2O MoO3 H2MoO4·H2O Fritted glass ZnSO4·H2O ZnSO4·7H2O ZnCl2 ZnO ZnSO4·4Zn(OH)2

Element (%)

Solubilitya

17 11 20 18 14 1.5–2.5 48 52 64 44 35 25 47 89 75 13 9

Soluble Soluble Soluble Soluble Soluble Sl. solubleb Soluble Soluble Soluble Soluble Soluble Soluble Soluble Insoluble Insoluble Soluble Soluble

33 19 14 23 5–14 5–9 6 10 2–6

Soluble Soluble Soluble Soluble Soluble Soluble Soluble Soluble Sl. soluble

23–28 26–28 17 31 41–68 5–12 2–10 39 54 66 53 0.1–0.4

Soluble Soluble Soluble Insoluble Insoluble Soluble Sl. soluble Soluble Soluble Sl. soluble Soluble Sl. soluble

36 23 48–50 50–80 55

Soluble Soluble Soluble Insoluble Sl. soluble continues

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Table XII—continued Element

Ni

Co

a b

Source Zn chelate Zn chelate Zn frits Ni chloride Ni nitrate Ni oxide Co sulfate Co nitrate

Formula Na2ZnEDTA NaZnEDTA Fritted glass NiCl2·6H2O Ni(NO3)2·6H2O NiO CoSO4·7H2O Co(NO3)2·6H2O

Element%

Solubilitya

14 9 4–9 25 20 79 21 20

Soluble Soluble Sl. soluble Soluble Soluble Insoluble Soluble Soluble

From Mortvedt (1991, 2000), and Martens and Westermann (1991). Slightly soluble.

on salt-affected soils often exhibit symptoms of Cl toxicity. Seed germination may be inhibited with high concentrations of Cl, so Cl fertilizers need to be applied in advance of planting (Bould et al., 1983). Copper deficiency can generally be corrected by applying 3.3 to 14.5 kg Cu ha−1 as broadcast CuSO4 (Martens and Westermann, 1991). The rates of banded CuSO4 required to correct Cu deficiency have been as low as 1.1 kg ha−1 for vegetables and as high as 6.6 kg Cu ha−1 for alfalfa, oat, and wheat. Copper deficiency can be corrected by banding or broadcasting Cu to soil or as foliar sprays. Lower rates of Cu application are required to correct Cu deficiency with banded compared to broadcast CuSO4. Foliar sprays are emergency measures, as Cu deficiency is most frequently corrected by soil applications (Murphy and Walsh, 1972) which are more effective than foliar sprays (Solberg et al., 1993). Soil application of CuSO4 is usually more effective than CuO, and Cu might need frequent applications when problems persist (Karamanos et al., 1986). The differences in the rates of Cu required to correct Cu deficiency vary with soil properties, crop requirement, and concentrations of extractable soil Cu. In semiarid regions, drying of top soil reduces Cu availability. Iron deficiency is corrected mainly by foliar sprays because soil applications are generally ineffective unless very high rates are applied. Typical Fe compounds used for foliar application to crops are FeSO4, Fe(NO3)2, and FeDTPA, and a 200 kg ha−1 FeSO4 rate was required to obtain maximum yields of annual crops (Mortvedt, 1991). More than one foliar spray and often three to four are needed during vegetative growth periods to obtain optimum production of crops like sorghum, soybean, and rice. Tree injection with ferric ammonium citrate (8% Fe) and seed treatment with FeEDDHA have had limited success in correcting Fe deficiency. Inorganic Fe sources applied to soils are rapidly converted to unavailable forms (oxidation of Fe2+ to Fe3+) in well-aerated soils, especially as soil pH increases. In Oxisols from central Brazil, Fe deficiency on upland rice was frequently reported where soil had been limed to pH ∼ 6 for the production of common bean

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and soybean in rotations (Fageria et al., 1994). Synthetic Fe chelates are generally the most effective Fe sources for soil and foliar applications, but their cost may be prohibitive. A common source of Fe applied to annual crops is FeSO4, but Fe chelates may be cost-effective if crops are of high value (fruits and berries). Fritted materials are sometimes used in acid soils to maintain Fe for plants (Martens and Westermann, 1991). A common source of Mn applied to soils and as foliar sprays is MnSO4. Soybean and rice commonly develop Mn deficiency during their growth on many soils. Optimum soybean yields were obtained with MnSO4 broadcast (14 kg ha−1) and band (3 kg ha−1) applied, and Mn deficiency was corrected by broadcasting MnSO4 (11 kg ha−1) or banding at half that rate or by timely foliar applications (1–2 kg ha−1) (Hatfield and Hickey, 1981). In other studies, 10 to 40 kg MnSO4 ha−1 was required to achieve maximum soybean yields (Anderson and Mortvedt, 1982). Manganese deficiency on soybeans grown in a Brazilian Cerrado Oxisol at pH 6.7 was corrected with applications of 15 mg MnSO4 kg−1 soil (Novais et al., 1989). Manganese deficiency on rice grown in a drained Histosol at pH ∼ 7 was alleviated with soil applications of ∼15 kg MnSO4 (Snyder et al., 1990). Seed applications of Mn also prevented Mn deficiency and provided near-maximum grain yields, and banded MnSO4 with seed has been equally as effective as sprayed Mn. Soil applications of Mn with acid-forming macronutrient fertilizers in neutral to high pH soils generally increase Mn effectiveness, and Mn deficiencies on plants grown in acid soils may be avoided by not over-liming. Both MnSO4 and MnO were effective as sources of Mn at rates of 20 kg Mn kg−1 for correcting Mn deficiency on soybeans grown in an Oxisol at pH 6.9 (Abreu et al., 1996). Chelated Mn (MnEDTA), MnSO4, and mangasol were equally effective for alleviating Mn deficiency on lupine (Brennan, 1996). Foliar applications of MnSO4 are effective for small grain cereals grown in calcareous and alkaline soils, which tend to dry during the growing season (Reuter et al., 1973). Soybean receiving 1.12 kg MnSO4 foliar sprays during early growth stages (V6) and again during late growth stages (R1) had higher yields than plants receiving single early sprays (Gettier et al., 1985). Multiple applications of foliar MnSO4 are usually superior to single applications on soybean (Cox, 1968). Molybdenum deficiency can be corrected by soil and foliar applications and by seed treatments. Since the availability of Mo increases as soil pH increases, liming acid soils to pH 6.5–7.0 will frequently prevent or correct Mo deficiencies (Martens and Westermann, 1991). The application of 0.01 to 0.5 kg Mo ha−1 will generally correct Mo deficiency. Sodium and/or ammonium molybdates are suitable sources for soil applications. Foliar applications of Mo have usually been more effective than soil applications for crops grown under dry conditions (Martens and Westermann, 1991). Foliar applications of 40 g Mo ha−1 increased bean growth and shoot N concentrations (Viera et al., 1998). High rates of seed-treated Mo

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could be toxic to rhizobia or my induce seedling injury (Sedberry et al., 1973). Even though excess Mo applications could lead to Cu deficiencies in animals (“molybdenosis”), this hazard is low since most Mo becomes relatively insoluble in well-drained soils (Martens and Westermann, 1991). Zinc deficiency can be corrected by either foliar or soil applications of ZnSO4 or ZnEDTA (Martens and Westermann, 1991). Foliar Zn is usually applied in emergencies to salvage crops when Zn deficiencies appear, and one foliar application is usually not adequate for correcting moderate to severe Zn deficiency. Maximum grain yields were obtained with foliar applications of ∼1 mg Zn kg−1 during the third and fourth weeks after plant emergence for maize grown in an Oxisol in central Brazil (Galr˜ao, 1994, 1996) and with 6 mg Zn kg−1 soil for upland rice grown in a greenhouse (Barbosa Filho et al., 1990). Applications of Zn either by broadcast or band usually are more effective than foliar applications (Murphy and Walsh, 1972). Zinc deficiency is common on land where subsoils have been exposed after land leveling, and these normally receive applications of farmyard manure to alleviate deficiencies and improve soil conditions (Martens and Westermann, 1991). Nickel is ubiquitous in soils, and most P fertilizers contain sufficient Ni for plant productivity, so Ni is not usually applied to soils. However, foliar applications have corrected Ni deficiency (Chamel and Newmann, 1987). Cobalt deficiency is usually controlled by soil broadcast applications (0.4 to 6 kg Co ha−1), foliar applications (500 mg Co L−1), and seed treatments (500 mg Co kg−1) (Raj, 1987; Reddy and Raj, 1975). Both sulfate and nitrate salts of Co have been used as fertilizers. 2. Residual Effects Knowledge concerning residual effects of applied micronutrient fertilizers is important to make sound and economic recommendations for succeeding crops. Micronutrient fertilizers have longer residual effects in high silt and clay than in sandy soils. Slightly soluble materials also have longer residual effects than highly soluble materials. Crop yields also determine residual micronutrient effects in soil. Information about long-term micronutrient effects is limited. Since crop recovery of micronutrients is relatively low, long-term residual effects might be expected. Broadcast applications of 2 kg B ha−1 as Borate-65 to a loam soil provided sufficient B for alfalfa and red clover for 2 years (Gupta, 1993). Recommendations for correcting Cu deficiency indicated a relatively high residual availability of applied Cu. For example, residual Cu was effective for 5 to 8 years after application for several crops (Martens and Westermann, 1991). Soil applications of Fe sources usually have no or only limited residual effects, since Fe2+ is rapidly converted to Fe3+ in aerated soils. Band applications of Fe at relatively high rates may be effective for more than 1 year provided tillage operations do not mix fertilizer

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with surrounding soil (Martens and Westermann, 1991). Manganese applied at 20 to 40 kg ha−1 to a sandy loam soil produced maximum soybean yields, but this Mn was insufficient to alleviate deficiency the next year (Gettier et al., 1984). However, optimum soybean yields occurred 2 years after broadcasting 30 kg Mn ha−1 on a clay loam soil (Mascagni and Cox, 1985). Residual effects have usually been higher for MnSO4 than for MnO (Abreu et al., 1996). The results regarding residual effects of Mo fertilization showed that effectiveness decreased ∼50% per year in some soils (Barrow et al., 1985). Broadcast applications of 34 kg ZnSO4 ha−1 were adequate to correct Zn deficiency on maize for 4 to 5 years, but banded Zn had to be applied at 6.6 kg ha−1 for ∼5 years to assure adequate residual Zn (Frye et al., 1978). Economical and long-term residual effects were also obtained for soil applications of Zn on wheat (Yilma et al., 1997).

C. PLANT IMPROVEMENT The steady increases in yields of major crops during the last half-century have been achieved through genetic improvement and improved management practices. The selection of improved genotypes adapted to wide ranges of climatic differences has contributed greatly to the overall gain in crop productivity during this time. In spite of these advances, mean yields of major crops are normally two- to fourfold below recorded maximum potentials (Baligar and Fageria, 1997). Newly developed genotypes of rice, maize, wheat, and soybean have been more efficient in the absorption and utilization of micronutrients compared to older cultivars (Clark and Duncan, 1991; Fageria, 1992). (See Table XV for scientific names of plant species.) The accumulation of micronutrients varies among plant species and cultivars/ genotypes within species (Marschner, 1995; Welch, 1986). Such differences among plant species/cultivars have been attributed to genetics, physiological/biochemical mechanisms, responses to climate variables, tolerance to pest and diseases, and responses to agronomic management practices. Genetic variations in plant acquisition of micronutrients have been reviewed (Brown et al., 1972; Duncan, 1994, Duncan and Carrow, 1999; Gerloff and Gabelman, 1983; Graham, 1984; Marschner, 1995). The development of genotypes/cultivars effective in the acquisition and use of micronutrients and with the desired agronomic characteristics is vital for improving yields and achieving genotypic adaptation to diversified environmental conditions and increased resistance to pests (Baligar and Fageria, 1997; Duncan, 1994; Graham, 1984). Plant and external factors affecting micronutrient use by plants and mechanisms and processes influencing genotypic differences in micronutrient efficiency have been summarized (Table XIII and Table XIV). Plant species differ considerably for B requirements and tolerance to deficient and toxic levels of B in soil (Fixen, 1993; Gupta, 1979; Rerkasem and Loneragan,

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Table XIII Plant and External Factors Affecting Micronutrient Use by Plantsa Plant factors

External factors

Genetic control Species/cultivar/genotype

Agronomic management practices Liming Crop rotation Incorporate crop residue, cover crops Soil Aeration/reducing conditions pH Organic matter levels and forms Temperature Moisture Status Texture/structure Compaction Fertilizers Source Timing, depth, method of placement, and application Use slow release form Elements Toxicities in acid (Al, Mn, pH) and saline (B, Cl) soils Deficiencies in acid (Cu, Zn, Mo) and alkaline (Zn, Fe, Mn, Cu) soils Others Arbuscular mycorrhizae, beneficial soil microbes Control weeds, diseases, and insects

Physiological Root length, density of main, laterals, and root hairs Higher shoot yield, harvest index, internal demand Higher physiological efficiency Higher nutrient uptake and utilization Excretion of H+, OH−, and HCO3− Biochemical Enzymes: rhodotorulic acid (Fe), ferroxamine b (Fe), ascorbic acid oxidase (Cu), carbonic acid anhydrase (Zn) Metallothionein (trace elements) Proline, aspharagine pinitol (salinity) Abscisic acid, proline (drought). Root exudates (citric, malic, transaconitic acids) Phytosiderophores Others Tolerance to stress (drought, acidity, alkalinity) Tolerance/resistance to diseases/pests Arial temperature, light quality, humidity

a

Baligar and Bennett (1986a,b), Baligar and Fageria (1997), Duncan (1994), and Fageria (1992).

1994). Plants with high requirements for B are alfalfa, apple, red beet, turnip, cabbage, and cauliflower (NRC, 1980). Genotypic differences for tolerance to high B have been observed in wheat, barley, annual medic, and field peas (Nable and Paull, 1991; Paull et al., 1992). Such differences sometimes are related to restricted B uptake and transport. For example, the susceptibility to B deficiency in tomato was due to the lack of plant ability to transport B from roots to shoots (Brown et al., 1972). The genetic variability for B uptake and leaf concentration was noted for maize (Gorsline et al., 1968). Sensitivity to high Cl concentrations varies widely among plant species and cultivars (Eaton, 1966), but Cl toxicity is more extensive worldwide than Cl deficiency,

238

FAGERIA et al. Table XIV Soil and Plant Mechanisms and Processes and Other Factors Influencing Genotypic Differences in Micronutrient Efficiency in Plants Grown under Mineral Stressesa

Nutrient acquisition Diffusion and mass flow in soil: buffer capacity, ionic concentration and properties, tortuosity, moisture, bulk density, temperature Root morphological factors: number, length, extension, density, root hair density Physiological: root/shoot ratio, root microorganisms (rhizobia, azotobacter, mycorrhizae), nutrient status, water uptake, nutrient influx and effux, nutrient transport rates, affinity for uptake (Km), threshold concentration (Cmin) Biochemical: enzyme secretion (phosphatases), chelating compounds, phytosiderophores, proton exudate, organic acid exudates (citric, malic, trans-aconitic, malic) Nutrient movement in root Transfer across endodermal cells and transport in roots Compartmentalization/binding within roots Rate of nutrient release to xylem Nutrient accumulation and remobilization in shoots Demand at cellular level and storage in vacuoles Retransport from older to younger leaves and from vegetative to reproductive tissues Rate of chelation in xylem transport Nutrient utilization and growth Nutrient metabolism at reduced tissue concentrations Lower element concentrations in supporting structures, particularly stems Elemental substitution (Fe for Mn, Mo for P, Co for Ni) Biochemical: peroxidase for Fe efficiency, ascorbic acid oxidase for Cu, carbonic anhydrase for Zn, metallothionein for metal toxicities Other factors Soil factors Soil solution: ionic equilibria, solubility, precipitation, competing ions, organic ions, pH, phytotoxic ions Physiochemical properties: organic matter, pH, aeration, structure, texture, compaction, moisture Environmental effects Intensity and quality of light (solar radiation) Temperature Moisture (rainfall, humidity, drought) Plant diseases, insects, and allelopathy a

From Baligar and Fageria (1997), Baligar et al. (1990), Duncan and Baligar (1990), Fageria (1992), and Gerloff (1987).

particularly in arid and semiarid regions. Plant tolerance to Cl has reported strawberry and pea to be very sensitive; lettuce, onion, maize, apple to be moderately sensitive; potato, cabbage, cauliflower, wheat, and ryegrass to be slightly tolerant; and red beet, spinach, rape and barley to be highly tolerant (Marschner, 1995). The genotypic differences in tolerance to Cu and other heavy metals are well known in certain species and ecotypes of natural vegetation (Woolhouse and

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Table XV Common and Scientific Names of Plant Species Mentioned in Text Alfalfa Amaranth, purple Apple Avocado Banana Barley Bean, broad/common/navy Bean, faba Bean, mung Beet, red and sugar Bluestem, big Cabbage Carrot Cauliflower Celery Chickpea Citrus Clover, red Clover, subterranean Clover, white Cotton Cowpea Cucumber Fescue, red Grape Lentil Lettuce Lupine, white Maize Mango Medic, annual (black) Millet, pearl Oat Onion Orchard grass Palm, oil Pea, common/field Peach Peanut (groundnut) Pear Pecan Pepper Potato, white Potato, sweet Radish

Medicago sativa L. Amaranthus cruentus L. Malus domestica Borkh. Persea americana Miller Musa paradisiaca L. Hordeum vulgare L. Phaseolus vulgaris L. Vicia faba L. Vigna radiata L. Beta vulgaris L. Andropogon gerardii Vitman Brassica oleracea var. capitata L. Daucus carota Hoffm. Brassica oleracea var. botrytis L. Apium graveolens L. Cicer arietinum L. Citrus spp. Trifolium pratense L. Trifolium subterraneum L. Trifolium repens L. Gossypium hirsutum L. Vigna unguiculata L. Walp. Cucumis sativus L. Festuca rubra L. Vitus vinifera L. Lens culinaris Medikus Lactuca sativa L. Lupinus albus L. Zea mays L. Mangifera indica L. Medicago spp. (Medicago lupulina L.) Pennisetum glaucum L. R. Br. Avena sativa L. Allium cepa L. Dactylis glomerata L. Elaeis oleifera Kunth Pisum sativum L. Prunus persica L. Arachis hypogaea L. Pyrus communis L. Carya illinoensis Wangenh. Capsicum annuum L. Solanum tuberosum L. Ipomoea batatas L. Raphanus sativus L. continues

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FAGERIA et al. Table XV—continued

Rape Rice Rutabaga/swede Rye Ryegrass, annual Sorghum Soybean Spinach Sugarcane Sunflower Swede/rutabaga Tobacco Tomato Turnip Wheat

Brassica napus L. Oryza sativa L. Brassica napus var. napobrassica Secale cereale L. Lolium multiflorum Lam. Sorghum bicolor (L.) Moench Glycine max (L.) Merr. Spinacia oleracea L. Saccharum officinarum L. Helianthus annuus L. Brassica napus var. napobrassica Nicotiana tabacum L. Lycopersicon lycopersicum (L.) Karsten Brassica rapa L. Triticum aestivum L.

Walker, 1981). It has been known for a long time that special flora (metallophytes) with a high tolerance to metals, including Cu, develop on outcrops of many contaminated mining sites (Marschner, 1995). The differences among plant species/cultivars for resistance to Fe deficiency and toxicity are extensive (Clark and Gross, 1986). Some plant species sensitive to Fe deficiency are apple, avocado, banana, citrus, grape, peach, pecan, bean, peanut, potato, sorghum, and soybean (Chen and Hadar, 1991). The differences among genotypes for Fe deficiency occur because of many physiological and biochemical differences. The recent classification of plants for differences in resistance to Fe deficiency has been categorized as Strategy I or Strategy II plants (R¨omheld and Marschner, 1986). That is, genotypes possessing Strategy I responses increase Fe solubility and uptake from the rhizosphere by enhanced reduction of Fe3+ to Fe2+, increased root H+ efflux and ATPase pumps to lower pH, increased root release of reductants capable of reducing Fe3+ to Fe2+, and increased production of organic acids, particularly citric and phenolics (Hughes et al., 1992). Most dicotyledonous and monocotyledonous plants, except those of the Poaceae (grass) family, exhibit these Fe deficiency stress traits. Genotypes of Poaceae exhibit Strategy II responses which are characterized by the production and release of Fe-solubilizing compounds (phytosiderophores) which complex sparingly soluble Fe3+ and make it available to plants (Hughes et al., 1992). Brown and Jolley (1988) and Jolley et al. (1996) extensively addressed mechanisms affecting Fe availability in different species of crops and plant physiological responses for genotypic evaluation of Fe efficiency associated with Strategy I and Strategy II plants. Selecting and breeding plants with resistance to Fe deficiency have been important for adapting plants for production on many Fe-deficient soils (Chen and Barak, 1982; Clark and Duncan, 1991, 1993; Clark et al., 1990; Rodriquez de

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Cianzio, 1991). The control of Fe deficiency is complicated in some plant species (multiple genes) and relatively simple in others (two genes), and good progress of achieving Fe deficiency resistance in some plant species has been made (Clark and Duncan, 1991, 1993; Clark et al., 1990). Improved germplasm for Fe deficiency has been released for bean, soybean, oat, and sorghum, with considerable progress being achieved with peanut, clover, bluestem grass, pepper, citrus, mango, and avocado (Rodriquez de Cianzio, 1991). Audeber and Sahrawat (2000) reported that the Fe-tolerant lowland rice cultivar “CK4” owed its superior performance under Fe-toxic conditions partly to avoidance (less Fe accumulation in leaves) and tolerance (superior photosynthetic potential in the presence of absorbed Fe in the leaves). Further, they stated that these mechanisms can be enhanced further through the application of P, K, and Zn to soil. Genotypic differences to Mo deficiency/toxicity have been noted (Marschner, 1995), and Mo toxicity tolerance has been closely related to the differences in translocation of Mo from roots to shoots (Marschner, 1995). Plant species and cultivars within species differ considerably in susceptibility to Mn deficiency when grown in low Mn soils (Marschner, 1995). Mechanisms responsible for cultivar differences for resistance to Mn deficiency are not known, but Marschner (1995) speculated that Mn oxidation/reduction reactions in the rhizosphere by roots and microorganisms were involved. Root exudates enhance the reduction of Mn oxides (Godo and Reisenauer, 1980). Both Mn deficiency and toxicity are common among plant species, and wide differences among plant species for resistance/tolerance to low and high Mn have been reported (Foy et al., 1988; Martens and Westermann, 1991; Reuter et al., 1988). Maize and rye are very susceptible to Mn deficiency, but oat, wheat, soybean, and peach are not (Reuter et al., 1988). The genotypic ability to tolerate Mn deficiency has been associated with root geometry, root excretion of substances (H+, reductants, Mn-binding ligands, microbial stimulants) to mobilize insoluble Mn, rates of Mn absorption at low soil Mn levels (low Km and high Vmax values), internal redistribution of Mn, and internal utilization or lower functional Mn requirements (Graham, 1984). Greater ranges of Mn in foliage of different plant species growing in the same soil were noted compared to Cu, Zn, and Fe, and these differences were attributed to species ability to acidify rhizosphere soil rather than with an internal Mn requirement (Gladstone and Loneragan, 1970). Genotypic differences were related to Mn acquisition from soil by rye and wheat (Marschner, 1988) and to geographic origin for barley (Graham, 1984), and not to differences in plant internal utilization and requirement. Some plant species grown in acid soils are more sensitive to Mn toxicity than others, and species differences to Mn toxicity have been reported for subterranean clover, bean, rice, tobacco, orchard grass, cotton, cowpea, apple, amaranth, and red fescue (Foy et al., 1988). Plants that are sensitive to Mn toxicity include cotton, field beans, alfalfa, cabbage, small grains, sugar beets, and pineapple (Martens

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and Westermann, 1991). Differential tolerance for Mn toxicity in plants has been associated with the oxidizing power of roots, uptake and rate of translocation from roots to shoots, entrapment of Mn in nonmetabolic centers, high internal tolerance to excess Mn, and distribution of Si, Cu, and Fe in tissue (Foy et al., 1988). Plant species/genotypes vary widely in resistance/tolerance to Zn-deficient or toxic soils (Graham and Rengel, 1993; Parker, 1997; Rashid and Fox, 1992; Takkar, 1993). The susceptibility of plants to Zn deficiency is high in cotton, bean, maize, and apple compared to pea, wheat, and oat. Maize, rice, lentil, chickpea, pea, and citrus are more sensitive to Zn deficiency than oilseed and cereal crops (Tiwari and Dwivedi, 1990). The differential responses among genotypes for Zn deficiency have also been reported for wheat, barley, oat, maize, sorghum, pearl millet, navy bean, potato, spinach, and soybean (Cakmak et al., 1997; Graham and Rengel, 1993; Takkar, 1993; Takkar and Walker, 1993). The differences in rice cultivars for Zn deficiency, especially those growing in high pH soil, were associated with the differences in susceptibility to HCO3− (Forno et al., 1975). Bicarbonate concentrations of 5 to 10 mM inhibited root growth of a “Zn-inefficient” rice cultivar, but stimulated root growth of “Zn-efficient” cultivars (Yang et al., 1994). Greater Zn acquisition in rice was casually related to the high HCO3− tolerance of roots (Yang et al., 1994). The differential susceptibility of common bean and soybean to Zn deficiency was associated with restricted translocation of Zn from roots to shoots (Ibrikci and Moraghan, 1993). The genotypic differences for “Zn efficiency” have been related to the effectiveness of absorption and translocation capacity of roots, ability of plants to avoid P toxicity when Zn deficiency occurs, root productivity of Zn mobilizing phytosiderophores, and production of seeds with high Zn contents (Graham and Rengel, 1993). Zinc deficiency is known to enhance the release of phytosideophores from roots of graminaceous species, and the release of phytosideophores by roots appears to be an adaptive response to Zn deficiency (Erenoglu et al., 2000). The rate of phytosiderophores released in triticale, rye, and bread wheat genotypes was not related to Zn efficiency or inefficiency. However, phytosiderophores had a role in Zn efficiency in barley cultivars, and it appears that phytosiderophores have a role in the solubility and mobility of Zn in the rhizosphere and within plant tissue (Erenoglu et al., 2000). The mechanisms associated with the differences for Zn deficiency operate in the soil as well as in the plant. Soil mechanisms for differential Zn at low levels include the differential ability of roots to sustain mycorrhizal infections, Zn mobilization and utilization, and Zn extraction from soil. Plant mechanisms include changes in rhizosphere pH, root uptake kinetics and transport, and root exudation of ion complexing and mobilization compounds (phytosiderophores). Crops also differ in susceptibility to toxic levels of Zn. In acid soils, most grasses (monocotyledons) are more tolerant than most dicotyledons, but this order is reversed for plants grown in alkaline soils, and leafy vegetables, legumes, and

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beet family plants are sensitive to high Zn while many dicotyledons tolerate toxic levels of Zn (Chaney, 1993). Bean and soybean cultivars also differ in tolerance to phytotoxic Zn (Chaney, 1993). Sugar beet and spinach are very susceptible to Ni toxicity, while barley, wheat, ryegrass, and broad bean are fairly resistant to Ni toxicity (Hewitt, 1983). The genotypic differences in tolerance to Co concentrations in shoots have been reported (Marschner, 1995).

D. MICROBIAL ASSOCIATIONS Beneficial soil microorganisms such as rhizobia, diazotrophic bacteria, and mycorrhizae may improve growth by enhancing atmospheric N2 fixation, suppressing pathogens, producing phytohormones, enhancing root surface areas to facilitate uptake of less mobile micronutrients, and mobilizing and solubilizing unavailable organic and inorganic mineral nutrients (Cattlelan et al., 1999; Marschner, 1995). Legumes would be unable to fix N2 without microorganisms like rhizobia, which have essential Co requirements (Ahmed and Evans, 1960). Many microorganisms produce siderophores, especially when grown under Fe deficiency conditions, which may enhance the plant acquisition of Fe (Crowley et al., 1987). Siderophores are large organic molecules [e.g., hydroxamates (amide functional groups) produced by fungi and bacteria and catecholates (aeromatic functional groups) produced by bacteria] that strongly and specifically bind metals, especially Fe3+ (Crowley et al., 1987; Germida and Siciliano, 2000; Lynch, 1990). Rhizosphere microorganisms may also be associated with differences among cultivars in their effectiveness to grow with low levels of some minerals. For example, a “Mn-efficient” wheat cultivar (high growth under Mn deficiency conditions) had a higher colonization of soil pseudomonads than “Mn-inefficient” cultivars, and a “Zn-efficient” cultivar had a higher colonization of nonpseudomonads than “Zn-inefficient” cultivars (Rengel et al., 1998). Mycorrhizal colonization of roots increases root surface areas to enhance root exploration of large soil volumes compared to uninfected roots and increases mineral nutrient uptake and plant tolerance to soil chemical constraints (acidity, alkalinity, salinity), toxic elements, and drought (Marschner, 1995). Mycorrhizal fungi and/or mycorrhizal roots have particularly increased acquisition of Cu, Fe, Mn, and Zn in plants grown under deficiency conditions (usually in alkaline soils) and decreased B, Fe, and Mn in plants grown under conditions where these minerals are excessive (usually in acidic soils) (Clark and Zeto, 2000; Marschner and R¨omheld, 1996). Mycorrhizae are also involved in the biological control of root pathogens and in nutrient cycling (solubilization, mineralization) (Marschner, 1995). Microbial interactions may also influence micronutrient mobility. Micronutrients react with microbial products (CO2, siderophores, organic compounds) and

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form microbial-mediated alterations in physical and chemical (pH, redox potentials) environments (Tate, 1987). Iron, Mn, and sometimes Cu are directly reduced by soil microbes or by soil humic acids (Tate, 1987). Several microbes involved in redox reactions in soil have been identified (Mullen, 1998). For example, Thiobacillus, Geobacter, Desulfovibrio, Pseudomonas, and Thiobacillus bacteria are involved in the oxidation of Fe2+ to Fe3+; Arthobacter, Leptothrix, Pseudomonas, and several other bacteria and fungi enhance oxidation of Mn2+ to Mn4+; and Bacillus, Geobacter, and Pseudomonas bacteria enhance Mn4+ reduction to Mn2+ (Paul and Clark, 1989). Noninfecting rhizosphere microorganisms may enhance plant micronutrient nutrition by improving growth and morphology of roots, physiology and development of plants, and micronutrient uptake processes by roots (Bowen and Rovira, 1991). Large numbers of microorganisms may enhance plant disease and insect infestations to reduce crop yields (Fageria, 1992; Lyda, 1981). Soilborne pathogens such as actinomycetes, bacteria, fungi, nematodes, and viruses lead to pathogenic stress and change the morphology and physiology of roots and shoots (Fageria, 1992; Fageria, Baligar, and Jones, 1997; Lyda, 1981). Such changes reduce plant ability to absorb and use micronutrients effectively. Diseases and insects mostly infect plant leaves (site of photosynthesis), and reduced photosynthetic activity results in a lower utilization of absorbed micronutrients (Fageria, 1992). Plant diseases are also greatly influenced by micronutrient deficiencies and/or toxicities (Huber, 1980). The severity of obligate and facultative parasites on plants is influenced by many micronutrients (Engelhard, 1990; Graham and Webb, 1991; Huber, 1980). The lack of Zn, B, Mn, Mo, Ni, Cu, and Fe in plant tissue can enhance various diseases on plants (Engelhard, 1990; Fageria, Baligar and Jones, 1997; Graham and Webb, 1991; Huber, 1980).

E. IMPROVED DISEASE AND INSECT RESISTANCE AND TOLERANCE Plant nutrition has always been an important component of disease control (Huber and Wilhelm, 1988). Mineral nutrients in plant tissue increase resistance by maximizing the inherent resistance of plants, facilitating disease escape through increased nutrient availability or stimulated plant growth, and altering external environments to influence survival, germination, and penetration of pathogens. Micronutrient concentrations in plants are important in host ability to resist or tolerate infectious pathogens. The tolerance of host plants to diseases is measured by the ability to maintain growth and/or yield in spite of infections (Turdgill, 1986). The resistance of the host plants is determined by plant ability to limit penetration, development, and/or reproduction of invading pathogens, and the resistance varies with species or genotype of the two organisms, plant age, and changes in the environment (Graham and Webb, 1991).

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The deficiencies of Cu, Fe, Mn, Mo, and Zn reduced growth and sporulation of the fungus Fusorium oxyspoum (Jones et al., 1990), while increased levels of soil Fe, Mn, and Zn benefitted the growth and sporulation of the pathogen. Take-all diseases of small grains from Gaeumannomyces graminis responded dramatically to the differences in micronutrient nutrition (Huber, 1990). Chlorine, Cu, Fe, Mn, and Zn in plants reduced take-all severity, while Mo increased disease severity. Adequate Cu and Mn could control white potato common scab caused by Streptomyces scabies, and Fe, Zn, and B had beneficial effects on reducing scab (Keinath and Loria, 1990). Boron sufficiency in plants reduced the incidence and severity of diseases, while B deficiency enhanced them. For example, brown-heart (water core) in radish and rutabaga roots, heart rot of beets, brown-heart rot of cauliflower, internal brown spot of sweet potato, and cracked stem of celery were enhanced when plants had insufficient B (Gupta, 1993). Boron sufficiency also reduced the incidence of club root in swede and other crucifers, fusarium in bean, tomato, and cotton, rhizoctonia infection in mung bean, pea, and cowpea, tobacco mosaic virus in bean and tomato, and yellow leaf curl virus in tomato (Graham and Webb, 1991). Chlorine tends to reduce the incidence of disease on many plants (Fixen, 1993; Marschner, 1995). For example, Cl particularly controlled stalk rot and northern leaf blight on maize, stripe rust and take-all on wheat, downy mildew on millet, and root rot on barley (Graham and Webb, 1991; Heckman, 1998). Powdery mildew and leaf rust diseases were suppressed in winter wheat with Cl applications at seven of nine experimental locations (Engel et al., 1994). Copper has been used extensively over time as a fungicide and suppresses many soilborne diseases. Soil applications of Cu decreased many fungal and bacterial diseases, including mildew on wheat and ergot on rye and barley (Graham and Webb, 1991). Iron decreased rust and smut infections on wheat and reduced Colletotrichum musae infections on banana, and foliar Fe sprays enhanced the resistance of apple and pear to Sphaeropsis malorum and tolerance of cabbage to Olpidium brassicae (Graham and Webb, 1991). Manganese increased the resistance and tolerance of plants to both root and foliar fungal and bacterial diseases. The effects of Mn on disease resistance occur over both Mn deficiency and sufficiency ranges of host plants (Graham and Webb, 1991). Manganese concentrations in host tissue commonly decrease as the incidence of disease increases, and the incidence of disease may be related to the reduced absorptive capacity of roots by pathogens and the immobilization of Mn by oxidation. Manganese availability in the rhizosphere and Mn concentrations in roots are important for manifestation of take-all severity. For example, increases in soil pH or using NO3–N versus NH4–N decreased the Mn availability and increased the take-all severity (Huber, 1990). Take-all on wheat was also reduced when seeds contained high compared to low Mn (McCay-Buis et al., 1995). Manganese was

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also effective in controlling other soilborne diseases such as potato common scab and verticillium wilt (Verticillum dahaliac) (Graham and Webb, 1991). Kleb wilt in cotton grown in acidic soil may be due to toxicity of Mn, Al, and possibly other acid soluble micronutrients (Bell, 1990). Even though the specific roles of Mo in protecting plants from diseases are unknown, the indications have been that Mo suppresses verticillium wilt in tomato (Graham and Webb, 1991). Zinc had decreased, increased, and no effects on plant susceptibility to diseases (Graham and Webb, 1991). Nickel salts were effective as fungicides against leaf and stem rusts on wheat (Graham and Webb 1991). The factors by which plants resist pests include physical (surface properties, hairs, color), mechanical (fibers, silicon), and chemical and/or biochemical (stimulants, toxins, repellants) properties (Marschner, 1995). Mineral nutrients can affect these factors to some degree. High amino acids in plants encourage the incidence of sucking parasites. Zinc deficiency can reduce protein synthesis which may lead to the high accumulation of amino acids. Negative relationships were noted between B contents in leaves of oil palm seedlings and attack by red spider mites (Rajaratnam and Hock, 1975). Boron was required for biosynthesis of cyanidin and was related to polyphenol production, which is involved in resistance against some insects (Marschner, 1995). Although Si has not been discussed as a micronutrient, high or adequate Si can restrict fungal and insect penetration of plant cells (and alleviate many diseases) to alleviate many insect and disease problems on plants (B´elanger et al., 1995; Epstein, 1994, 1999; Menzies and B´elanger, 1996; Savant et al., 1997, 1999). Silicon in epidermal cell walls acts as a mechanical barrier to insect and fungal attacks. The importance of Si in insect and disease resistance has been studied extensively in rice, sugarcane, and cucumber (B´elanger et al., 1995; Menzies and B´elanger, 1996; Savant et al., 1997, 1999).

VI. CONCLUSION The incidence of micronutrient deficiencies in crops has increased markedly in recent years due to intensive cropping, loss of top soil by erosion, losses of micronutrients through leaching, liming of acid soils, decreased proportions of farmyard manure compared with chemical fertilizers, increased purity of chemical fertilizers, and use of marginal lands for crop production. Micronutrient deficiency problems are also aggravated by a high demand of modern crop cultivars. Increases in crop yields from application of micronutrients have been reported in many parts of the world. Factors such as pH, redox potential, biological activity, SOM, cation-exchange capacity, and clay contents are important in determining the availability of micronutrients in soils. Further, root-induced changes in the rhizosphere affect the availability of micronutrients to plants. Major root-induced

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changes in the rhizosphere are pH, reducing capacity, redox potentials, and root exudates that mobilize sparingly soluble mineral nutrients. Root exudates may make elements like Fe more available, but they may also produce water-soluble metal chelating agents which reduce metal activity with roots. Compared to macronutrients, micronutrients are required for crop growth in lower amounts and serve mainly as constituents of prosthetic groups in metalloproteins and/or as activators of enzyme reactions. Micronutrients in crop production are important, and micronutrients deserve consideration similar to that of macronutrients. Micronutrient application rates range from 0.2 to 100 kg ha−1, depending on the micronutrient, crop requirement, and method of application. Higher rates are required for broadcast than for banded applications on soil or as foliar sprays. Because recommended application rates of micronutrients are low, most micronutrient sources are combined with macronutrient fertilizers for application to soil. This practice assures uniform micronutrient application. The development micronutrient-efficient and/or tolerant-resistant genotypes appears promising for improving future crop production. Additional information is needed to improve micronutrient recommendations, especially for determining long-term availability, and to evaluate macronutrient fertilizer effects on micronutrient availability. Considerable information about critical deficiency levels of micronutrients is available, but information about critical toxic levels is limited. Information about the interactions of micronutrients with other minerals is also needed.

ACKNOWLEDGMENTS The authors are grateful to Drs. V. D. Jolley, L. M. Shuman, D. C. Martens, G.Ba˜nuelos, and C. D. Foy for their critical review and valuable suggestions for the manuscript. We also thank Dr. L. W. Zelazny for providing information on major soil minerals containing micronutrients.

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