Handbook of Plant Nutrition - chapter 11 pps

Theequilibrium concentration of Fe3 ⫹in calcareous soil solution at pH 8.3 is 10⫺19mM 22, whichgives noticeable iron deficiency in plants not adapted to these conditions.. 11.4 DIAGNOSIS

11 Iron

Volker Römheld University of Hohenheim, Stuttgart, Germany

Miroslav Nikolic University of Belgrade, Belgrade, Serbia

CONTENTS

11.1 Historical Information 329

11.1.1 Determination of Essentiality 329

11.2 Functions in Plants 330

11.3 Forms and Sources of Iron in Soils 330

11.4 Diagnosis of Iron Status in Plants 332

11.4.1 Iron Deficiency 332

11.4.2 Iron Toxicity 332

11.5 Iron Concentration in Crops 335

11.5.1 Plant Part and Growth Stage 335

11.5.2 Iron Requirement of Some Crops 335

11.5.3 Iron Levels in Plants 336

11.5.3.1 Iron Uptake 336

11.5.3.2 Movement of Iron within Plants 338

11.6 Factors Affecting Plant Uptake 339

11.6.1 Soil Factors 339

11.6.2 Plant Factors 343

11.7 Soil Testing for Iron 344

11.8 Fertilizers for Iron 344

References 345

11.1 HISTORICAL INFORMATION

11.1.1 DETERMINATION OF ESSENTIALITY

Julius von Sachs, the founder of modern water culture experiments, included iron in his first nutri-ent cultures in 1860, and Eusèbe Gris, in 1844, showed that iron was essnutri-ential for curing chlorosis

in vines (1,2) Sachs had already shown that iron can be taken up by leaves, and within a few years

L Rissmüller had demonstrated that foliar iron is obviously translocated by phloem out of leaves

before leaf fall in European beech (Fagus sylvatica L.) The early developments in the study of iron

in plant nutrition were summarized by Molisch in 1892 (3)

It was another 100 years before the principal processes of the mobilization of iron in the rhizosphere started to be understood (4–8)

329

The heme proteins contain a characteristic heme iron–porphyrin complex, and this acts as aprosthetic group of the cytochromes These are electron acceptors–donors in respiratory reactions.Other heme proteins include catalase, peroxidase, and leghemoglobin.

Catalase catalyzes the conversion of hydrogen peroxide into water and O2(reaction A), whereasperoxidases catalyze the conversion of hydrogen peroxide to water (reaction B):

AH⫹ AH ⫹ H2O2→A⫺ A ⫹ 2H2OCatalase has a major role in the photorespiration reactions, as well as in the glycolate pathway, and

is involved in the protection of chloroplasts from free radicals produced during the water-splittingreaction of photosynthesis The reaction sequence of peroxidase shown above includes cell wallperoxidases, which catalyze the polymerization of phenols to form lignin Peroxidase activity isnoticeably depressed in roots of iron-deficient plants, and inhibited cell wall formation andlignification, and accumulation of phenolic compounds have been reported in iron-deficient roots

As well as being a constituent of the heme group, iron is required at two other stages in its facture It activates the enzymes aminolevulinic acid synthetase and coproporphorinogen oxidase Theprotoporphyrin synthesized as a precursor of heme is also a precursor of chlorophyll, and although iron

manu-is not a constituent of chlorophyll thmanu-is requirement, and the fact that it manu-is also required for the sion of Mg protoporphyrin to protochlorophyllide, means that it is essential for chlorophyll biosynthe-sis (10) However, the decreased chloroplast volume and protein content per chloroplast (11) indicatethat chlorophyll might not be adequately stabilized as chromoprotein in chloroplasts under iron

conver-deficiency conditions, thus resulting in chlorosis

Along with the iron requirement in some heme enzymes and its involvement in the ture of heme groups in general, iron has a function in Fe-S proteins, which have a strong involve-ment with the light-dependent reactions of photosynthesis Ferredoxin, the end product ofphotosystem I, has a high negative redox potential that enables it to transfer electrons to a number

manufac-of acceptors As well as being the electron donor for the synthesis manufac-of NADPH in photosystem I, itcan reduce nitrite in the reaction catalyzed by nitrite reductase and it is an electron donor for sulfitereductase

11.3 FORMS AND SOURCES OF IRON IN SOILS

Iron occurs in concentrations of 7,000 to 500,000 mg kg⫺1in soils (12), where it is present mainly

in the insoluble Fe(III) (ferric, Fe3 ⫹) form Ferric ions hydrolyze readily to give Fe(OH)2⫹,Fe(OH)3, and Fe(OH)4⫺, with the combination of these three forms and the Fe3 ⫹ions being the totalsoluble inorganic iron, and the proportions of these forms being determined by the reaction (13):

Fe(OH)3(soil)⫹ 3H⫹lFe3 ⫹⫹ 3H2O

With an increase in soil pH from 4 to 8, the concentration of Fe3 ⫹ions declines from 10⫺8to 10⫺20M.

As can be seen from Figure 11.1, the minimum solubility of total inorganic iron occurs between pH7.4 and 8.5 (14)

The various Fe(III) oxides are major components of a mineral soil, and they occur either as agel coating soil particles or as fine amorphous particles in the clay fraction Similar to the clay col-loids, these oxides have colloidal properties, but no cation-exchange capacity They can, however,bind some anions, such as phosphate, particularly at low pH, through anion adsorption For this rea-son, the presence of these oxides interferes with phosphorus acquisition by plants, and in soils of

pH above 6, more than 50% of the organically bound forms of phosphate may be present as Fe(Al)-P complexes (15)

humic-Although Fe(III) oxides are relatively insoluble in water, they can become mobile in the presence

of various organic compounds As water leaches through decomposing organic matter, it moves theFe(III) oxide downwards, particularly at acidic pH, so that under such conditions podzols form Theiron is essentially leached from the top layers of soil as iron–fulvic acid complexes and forms an ironpan after precipitation lower down at higher pH The upper layers are characteristically light in color,

as it is the gel coating of Fe(III) oxide that, in conjunction with humus, gives soils their tic color However, in soils in general, the intensity of the color is not an indication of iron content.These organic complexes tend to make iron more available than the thermodynamic equilibriumwould indicate (16), and in addition to iron-forming complexes with fulvic acid, it forms complexeswith microbial siderophores (13), including siderophores released by ectomycorrhizal fungi (17) Awater-soluble humic fraction extracted from peat has been shown to be able to form mobile com-plexes with iron, increasing its availability to plants (18)

characteris-In soils with a high organic matter content the concentration of iron chelates can reach 10⫺4to

10⫺ 3M (17,18) However, in well-aerated soils low in organic matter, the iron concentration in thesoil solution is in the range of 10⫺8to 10⫺ 7M, lower than is required for adequate growth of mostplants (13)

Under anaerobic conditions, ferric oxide is reduced to the Fe(II) (ferrous) state If there areabundant sulfates in the soil, these also become oxygen sources for soil bacteria, and black Fe(II)

16 14 12 10 8 6 4

pH

Fe3+

Fe(OH) 3

Total soluble inorganic Fe

FIGURE 11.1 Solubility of inorganic Fe in equilibrium with Fe oxides in a well-aerated soil The shaded

zone represents the concentration range required by plants for adequate Fe nutrition (Redrawn from Römheld,

V., Marschner, H., in Advances in Plant Nutrition, Vol 2, Praeger, New York, 1986, pp 155–204 and Lindsay, W.L., Schwab, A.P., J Plant Nutr., 5:821–840, 1982.)

sulfide is formed Such reactions occur when a soil becomes waterlogged, but on subsequentdrainage the Fe(II) iron is oxidized back to Fe(III) compounds Alternate bouts of reduction and oxi-dation as the water table changes in depth give rise to rust-colored patches of soil characteristic ofgleys Ferrous iron, Fe2 ⫹, and its hydrolysis species contribute toward total soluble iron in a soilonly if the sum of the negative log of ion activity and pH together fall below 12 (equivalent to Eh

of ⫹260 mV and ⫹320 mV at pH 7.5 and 6.5, respectively) (13,14) It is likely that the presence ofmicroorganisms around growing roots causes the redox potential in the rhizosphere to drop because

of the microbial oxygen demand, and this would serve to increase concentrations of Fe2 ⫹ions forplant uptake (21)

Because the solubility of Fe3 ⫹and Fe2 ⫹ions decreases with increase in pH, growing plants oncalcareous soils, and on soils that have been overlimed, gives rise to lime-induced chlorosis Theequilibrium concentration of Fe3 ⫹in calcareous soil solution at pH 8.3 is 10⫺19mM (22), whichgives noticeable iron deficiency in plants not adapted to these conditions It has been estimated that

up to 30% of the world’s arable land is too calcareous for optimum crop production (23,24).Iron deficiency can also arise from excess of manganese and copper Most elements can serve

as oxidizing agents that convert Fe2 ⫹ions into the less soluble Fe3 ⫹ions (25), and excess ganese in acid soils can give rise to deficiencies of iron although it would otherwise be present inadequate amounts (26)

man-Corn (Zea mays L.) and sugarcane (Saccharum o fficinarum L.) may show iron deficiency

symp-toms when deficient in potassium It seems that under these circumstances iron is immobilized inthe stem nodes, a process that is accentuated by good phosphorus supply (27) Iron can bind asignificant proportion of phosphate in well-weathered soil (as the mineral strengite), and as this sub-stance is poorly soluble at pH values below 5, iron contributes to the poor availability of phospho-rus in acid soils (25)

11.4 DIAGNOSIS OF IRON STATUS IN PLANTS

11.4.1 IRON DEFICIENCY

The typical symptoms of iron deficiency in plants are chlorotic leaves Often the veins remain greenwhereas the laminae are yellow, and a fine reticulate pattern develops with the darker green veinscontrasting markedly with a lighter green or yellow background (Figure 11.2, see also Figure 1.1 inChapter 1) In cereals, this shows up as alternate yellow and green stripes (Figure 11.3) Iron

deficiency causes marked changes in the ultrastructure of chloroplasts, with thylakoid grana beingabsent under extreme deficiency and the chloroplasts being smaller (27,28) As iron in older leaves,mainly located in chloroplasts, is not easily retranslocated as long as the leaves are not senescent,the younger leaves tend to be more affected than the older leaves (Figure 11.4) In extreme casesthe leaves may become almost white Plant species that can modify the rhizosphere to make ironmore available can be classified as iron-efficient and those that cannot as iron-inefficient It is among

the iron-inefficient species that chlorosis is most commonly observed

11.4.2 IRON TOXICITY

Iron toxicity is not a common problem in the field, except in rice crops in Asia (29) It can also occur

in pot experiments, and in cases of oversupply of iron salts to ornamental plants such as azaleas.The symptoms in rice, known as ‘Akagare I’ or ‘bronzing’ in Asia, include small reddish-brownspots on the leaves, which gradually extend to the older leaves The whole leaf may turn brown, andthe older leaves may die prematurely (29) In other species, leaves may become darker in color androots may turn brown (29) In rice, iron toxicity seems to occur above 500 mg Fe kg⫺1leaf dryweight (30) (Figure 11.5)

FIGURE 11.2 Iron-deficient cucumber (Cucumis sativus L.) plant (Photograph by Allen V Barker.) (For a

color presentation of this figure, see the accompanying compact disc.)

FIGURE 11.3 Iron-deficient corn (Zea mays L.) plant (Photograph by Allen V Barker.) (For a color

pres-entation of this figure, see the accompanying compact disc.)

FIGURE 11.5 Symptoms of iron toxicity in lowland rice (Oryza sativa L.) in Sri Lanka as a consequence of

decreased redox potential under submergence (Photograph by Volker Römheld.) (For a color presentation of this figure, see the accompanying compact disc.)

FIGURE 11.4 Iron-deficient pepper (Capsicum annuum L.) plant The young leaves are yellow, and the older

leaves are more green (Photograph by Allen V Barker.) (For a color presentation of this figure, see the panying compact disc.)

accom-11.5 IRON CONCENTRATION IN CROPS

11.5.1 PLANT PART AND GROWTH STAGE

Most of the iron in plants is in the Fe(III) form (11) The Fe(II) form is normally below the tion level in plants (31) A high proportion of iron is localized within the chloroplasts of rapidlygrowing leaves (10) One of the forms in which iron occurs in plastids is as phytoferritin, a protein

detec-in which iron occurs as a hydrous Fe(III) oxide phosphate micelle (9), but phytoferritdetec-in is also found

in the xylem and phloem (32) It also occurs in seeds, where it is an iron source that is degradedduring germination (33) However, in general, concentrations of iron in seeds are lower than in thevegetative organs

A large part of the iron in plants is in the apoplast, particularly the root apoplast Most of thisroot apoplastic pool is in the basal roots and older parts of the root system (34) There is also anoticeable apoplastic pool of iron in the shoots

In the iron hyperaccumulator Japanese blood grass (Imperata cylindrica Raeuschel), iron

accu-mulates in rhizomes and leaves in mineral form, in the rhizomes in particular as jarosite,KFe3(OH)6(SO4)2, and in the leaves probably as phytoferritin (35) In the rhizome this accumula-tion is in the epidermis and the xylem, and in the leaves it is in the epidermis

11.5.2 IRON REQUIREMENT OF SOME CROPS

Iron deficiency can be easily identified by visible symptoms, so this observation has made tative information on adequate concentrations of iron in plants more scarce (Table 11.1) (29)

High soil water content

Low soil temperature

Soil factors

Low O2concentration

High soil compaction

High heavy metal content

Management factors

Inadequate assimilate delivery and late vintage (harvest) Weakness chlorosis, stress chlorosis

Plant factors

Low root growth

High shoot:root dry matter ratio

Low Fe e fficiency

Source: From Kirkby, E.A., Römheld, V Micronutrients in Plant Physiology: Functions, Uptake and Mobility Proceedings

No 543, International Fertiliser Society, Cambridge, U.K., December 9, 2004, pp 1–54.

Furthermore, the so-called chlorosis paradox gives confusing results when critical levels are beingdetermined This confusion seems to be brought about by restricted leaf expansion due to shortage

of iron, giving rise to similar concentrations of iron in the smaller, chlorotic leaves as in healthy

green leaves (36) This paradox has been described in grapevine (Vitis vinifera L.) (37,38) and peach (Prunus persica Batsch) (39).

In general, the deficiency range is about 50 to 100 mg kg⫺1depending on the plant species andcultivars (Table 11.2) (28) This range is somewhat complex to determine, as iron-efficient plantspecies are able to react to low availability of iron by employing mechanisms for its enhanced acqui-sition (see below), whereas iron-inefficient species are more dependent on adequate supplies of ironbeing readily available In fact, it is apparent from simple calculations that plants must employ root-induced mobilization of iron to obtain enough element for normal growth (28) Calculations based onthe iron concentration of crops at harvest compared with the concentration of iron in soil water indi-cate an apparent shortfall in availability of a factor of approximately 2000, and calculations based onthe iron concentration of crops at harvest and their water requirements indicate a shortfall of a factor

of approximately 36,000 Both are very crude calculations, but they clearly indicate that the presence

of plants, at least iron-efficient plants, makes iron more available in the soil than would be expected.The data indicate a requirement of iron for an annual crop of 1 kg ha⫺1year⫺1, but even for tree speciesthe requirement is considerable It has been estimated that for a peach tree in northeastern Spain, theamount of iron in the prunings in particular, but also lost in the harvested fruit, in leaf and flowerabscission and immobilized in the wood, is between 1 and 2 g per tree per year (40)

11.5.3 IRON LEVELS IN PLANTS

In Strategy 1 plants, one of the major responses to iron deficiency is the acidification of the zosphere, brought about by differential cation–anion uptake (49), the release of dissociable reduc-tants (8,50) and particularly by the action of an iron-deficiency-induced proton pump in theplasmalemma of rhizodermis cells of apical root zones (51) This acidification of the rhizosphereserves to make iron more available and to facilitate the required Fe(III)-chelate reductase activity(52) There is also an enhanced growth of root hairs (53) and the development of structures liketransfer cells in the rhizodermis (10) as a response to iron deficiency

rhi-In chickpea (Cicer arietinum L.) subjected to iron deficiency, anion and cation uptake wereshown to be depressed, but anion uptake was depressed more than cation uptake (54) This effectgives rise to excess cation uptake, with consequent release of H⫹ions in a direct relationship to theextent of the cation–anion imbalance The origin of the H⫹release in such circumstances could bethrough enhanced PEP carboxylase activity (55)

The release of reductants increases the reduction of Fe3 ⫹to Fe2 ⫹in the apoplast, and has beenlinked to compounds such as caffeic acid (56,57) These may reduce Fe3 ⫹to Fe2 ⫹ions, and alsochelate the ions either for uptake or for reduction on the plasmalemma Such reduction of Fe3 ⫹

on the plasma membrane involves an iron-chelate reductase It was thought at one time that thereare two forms of such reductases, a constitutive form that works at a low capacity and is contin-uously present, and an inducible form that works with high capacity and is induced under iron

deficiency (10) However, in tomato (Lycopersicon esculentum Mill.), iron deficiency gives

rise to increased expression of constitutive FeIII-chelate reductase isoforms in the root malemma (58) Action of the FeIII-chelate reductase is the rate-limiting step of iron acquisition ofStrategy 1 plants under deficiency conditions (59–61) Genes encoding for proteins in FeIII-chelate reductase and involved with the uptake of Fe2 ⫹in Fe-deficient plants have been identified

plas-in the Strategy 1 plant Arabidopsis thaliana, and have been named AtFRO2 and AtIRT1,

respec-tively (62,63)

In Strategy 2 plants the phytosiderophores, nonprotein amino acids such as mugineic acid (64),are released in a diurnal rhythm following onset of iron deficiency (43,52) This release occurs par-ticularly in the apical regions of the seminal and lateral roots (65) The phytosiderophores form sta-ble complexes with Fe3 ⫹ions, and these complexes are taken up by a constitutive transporter in theplasmalemma of root cells (66) Activity of this transporter also increases during iron deficiency

Mutants such as corn (Zea mays L.) ys1/ys1 are very susceptible to iron chlorosis (44).

In the Strategy 1 species cucumber (Cucumis sativus L.), Fe3 ⫹attached to the water-soluble humicfraction is apparently reduced by the plasmalemma reductase, allowing uptake to occur (67,68),

whereas in Strategy 2 barley (Hordeum vulgare L.), there is an indirect method for uptake of this Fe3 ⫹component that involves ligand exchange between the humic fraction and phytosiderophores released

in response to iron deficiency (68) Uptake of iron then occurs as a Fe(III)–phytosiderophore complex

In Strategy II plants, iron deficiency also leads to a small increase in the capacity to take up Fe2 ⫹,uptake previously thought only to occur in Strategy 1 plants (69)

It has been suggested in the past that the large root apoplastic pool of iron could be a source ofiron for uptake into plants under iron deficiency However, the apoplastic pool occurs largely in theolder roots (34), yet the mobilization of rhizosphere iron and the uptake mechanisms that areinduced under iron deficiency stress occur in the apical zones of the roots, so this seems unlikely(70) The Strategy 1 and Strategy 2 mechanisms are switched on by mild iron deficit stress, althoughunder severe deficiency they become less effective They are switched off within a day of resump-tion of iron supply to the plant

The various iron transporters in plant cells have been well characterized They includeNramp3 transporters on the tonoplast, and IRT1, IRT2 and Nramp transporters on the plas-malemma (71) Nramp (natural resistance associated macrophage proteins) transporters areinvolved in metal ion transport in many different organisms, and in Arabidopsis roots, three

different Nramps are upregulated under iron deficiency A model of iron transport in Arabidopsis

has been shown elsewhere (72)

The transporter used by Strategy 1 plants is an AtIRT1 transporter, whereas Strategy 2 plantstake up the phytosiderophore–Fe(III) complex by ZmYS1 transporters (44,45)

Uptake of zinc, and possibly manganese and copper also, may increase in Strategy 2 plantsunder iron deficiency, because although the iron-phytosiderophore transporter is specific to ironcomplexes, the presence of the phytosiderophores in the rhizosphere may increase the availability

of these other ions both in the rhizosphere itself and in the apoplast (73)

As well as uptake through roots, iron is able to penetrate plant cuticles, at least at 100% ity Chelates of Fe3 ⫹ were shown to penetrate cuticular membranes from grey poplar (Populus x Canescens Moench.) leaves without stomata with a half-time of 20 to 30 h (74), although at 90%

humid-humidity Fe3 ⫹chelated with lignosulfonic acid was the only chelate tested that still penetrated themembrane Sachs himself showed that iron is taken up by plants after application to the foliage, andiron chelates have been applied to foliage to correct iron deficiencies because inorganic iron saltsare unstable and phytotoxic (see (3)) Fe(III) citrate and iron-dimerum have been found to penetrate

the leaves of chlorotic tobacco (Nicotiana tabacum L.) plants, and to be utilized by the cells (75),

but it is the chelated forms of iron that enter most effectively

11.5.3.2 Movement of Iron within Plants

Once taken up by root cells, iron moves within cells and between cells The understanding of ironhomeostasis at the subcellular level is incomplete, and the role of the vacuole is uncertain A car-rier called AtCCC1 may transport iron into vacuoles, and AtNRAMP3 and AtNRAMP4 are candi-dates for transporting it out (72) Of the cellular organelles, mitochondria and chloroplasts have ahigh requirement for iron, and the chloroplasts may be sites of storage of iron (76) Transport intochloroplasts is stimulated by light (77), and it occurs in the Fe(II) form (78)

Knowledge of the movement of iron between cells is also incomplete Experiments in which

59Fe-labelled iron-phytosiderophores were fed to roots of intact corn plants for periods of up to 2 hdemonstrated intensive accumulation of iron in the rhizodermis and the endodermis (72,79) Thisaccumulation was higher with iron deficiency stress, and probably reflected the role of increasednumber of root hairs and increased expression of the ZmYS1 iron-phytosiderophore transporter.From the endodermis, the iron is loaded into the pericycle and from there into the xylem Verylittle is known about these processes Once in the shoots, much of the iron is present in the apoplast,from where it is loaded into the cytoplasm and into the organelles where it is required It was

Strategy 1: Dicotyledons and nongraminaceous plant species

Strategy 2: Graminaceous plant species

FIGURE 11.6 Strategies for acquisition of Fe in response to Fe deficiency in Strategy 1 and Strategy 2

plants (Redrawn from Römheld, V., Schaaf, G., Soil Sci Plant Nutr., 50:1003–1012, 2004.)

thought at one time that high soil pH would raise shoot apoplastic pH and that this action wouldmake iron unavailable for transport into leaf cells However, this is not the case, as high root zoneHCO3⫺has been shown not to increase apoplastic pH of leaves in both nutrient-solution-grownsunflower (Helianthus annuus L.) and field-grown grapevine (Vitis vinifera L.) (80), a result that is

also in agreement with recent experiments of Kosegarten et al (81,82) In experiments ongrapevine, the presence of bicarbonate in the uptake medium was shown to inhibit uptake of ironand its translocation to the shoots, primarily by inhibiting the Fe(III) reduction capacity of the roots(83) Also, the recently discussed role of nitrate in iron inactivation in leaves and induction ofchlorosis due to an assumed increased leaf apoplast pH (82) could not be confirmed (84) Probably,this nitrate-induced chlorosis in solution-cultured sunflower plants is a consequence of an impedediron acquisition by roots as a consequence of a nitrate-induced pH increase at the uptake sites of theroots

Movement of iron salts in phloem is obviously possible as Rissmüller observed retranslocation

of iron from senescent leaves of beech trees long ago (3) However, it is usually thought that iron

deficiency symptoms occur in young leaves rather than in old leaves because iron is not easilyretranslocated in nonsenescent plants However, such retranslocation is not confined to the senes-

cent leaves of trees, as it has also been observed to occur out of young leaves of Phaseolus vulgaris

subjected to iron deficiency (85,86)

Nicotianamine seems to be involved in phloem loading for retranslocation of iron and possibly

in phloem unloading and uptake of iron into young leaves and reproductive organs The maizeZmYS1 protein not only mediates transport of iron–phytosiderophore complexes (87,88), but

experiments on this transporter in yeast and Xenopus have shown that it can also transport

Fe(II)-nicotianamine and Fe(III)-Fe(II)-nicotianamine (88) The AtYSL2 homolog of this protein has been

impli-cated in lateral movement of iron in the vascular system of Arabidopsis thaliana (89,90), and its

OsYSL2 homolog in rice has been suggested to be involved in transport of Fe(II)-nicotianamine inphloem loading and translocation of metals into the grain (91) Expression of a nicotianamine syn-

thase gene from Arabidopsis thaliana in Nicotiana tabacum gave increased levels of nicotianamine,

more iron in the leaves of adult plants, and improvement in the iron use efficiency of plants grownunder iron deficiency stress (92)

11.6 FACTORS AFFECTING PLANT UPTAKE

One factor that may contribute to rhizosphere pH changes, other than the underlying substrate,

is the nitrogen source When plants take up nitrate as their predominant nitrogen source, they linize the rhizosphere and this contributes to iron deficiency stress (84,93,94) It has been suggestedthat nitrate nutrition could actually raise the pH in the leaf apoplast, making iron less available fortransport into leaf cells However, this assumption was not experimentally confirmed (see Section11.5.3.2)

alka-Chlorosis in plant species with Strategy 1 is made worse by high soil moisture, particularly oncalcareous soils, because of elevated concentrations of bicarbonates A peach tree that was overir-rigated in an orchard on a calcareous soil developed bicarbonate-induced chlorosis, whereas a treethat received proper irrigation showed no chlorosis (Figure 11.7) In addition, anaerobiosis maymake root responses to iron deficiency stress more difficult (13) Organic matter content of the soil