Content-Type: multipart/related; start=; boundary=----------ESkxXakrTjRzpol2uN2eJ1 Content-Location: http://home.infinet.net/teban/iron/ironw.html Subject: =?utf-8?Q?FACTORES=20INVOLUCRADOS=20EN=20LA=20ABSORCION=20Y=20ASIMILACION=20DE=20HIERRO=20POR=20LAS=20PLANTAS?= MIME-Version: 1.0 ------------ESkxXakrTjRzpol2uN2eJ1 Content-Disposition: inline; filename=ironw.html Content-Type: text/html; charset=iso-8859-1; name=ironw.html Content-Id: Content-Location: http://home.infinet.net/teban/iron/ironw.html Content-Transfer-Encoding: 8bit FACTORES INVOLUCRADOS EN LA ABSORCION Y ASIMILACION DE HIERRO POR LAS PLANTAS
ABSORPTION and ASSIMILATION of IRON in PLANTS

DR. ADALBERTO BENAVIDES MENDOZA

DEPARTAMENTO DE HORTICULTURA, UNIVERSIDAD AUTONOMA AGRARIA ANTONIO NARRO

JULY, 1999

translation by Roger Miller
Last Modified:

1. INTRODUCTION

Most of a third of the world population suffers iron (Fe) deficiency, but the parts of the population most affected are women of reproductive age and children (Robinson et al. 1999).  Recent studies that connect Fe deficiency with deficient cognitive development emphasize the impact of the problem.   Plants are the principle source of iron in the majority of diets, so assuring consumption of vegetables with an adequate level of iron constitutes an essential part of the strategy for improving the level of human nutrition (Theil et al., 1997).  The aforesaid gains greater significance when refering to agricultural systems in areas with calcareous soils where the crops probably have suboptimum levels of Fe.

A characteristic problem associated with cultivation in calcareous soils is the condition called iron chlorosis, a consequence of extreme iron deficiency and whose most characteristic symptom is intervenal chlorosis which is corrected with application of Fe in forms available to plants (Emery, 1982).  Calcareous soils don't lack Fe per se, but its availability is just the same limited.  On the other hand the condition of iron chlorosis isn't exclusive to calcareous soils,  although most of the problems of this type are found in regions with this type of soil (Brown and Jolley, 1989).

Calcareous soils comprise approximately a third of the land surface and are found predominantly in regions that receive less than 500 mm of annual precipitation.  The important characteristics of a calcareous soil are a high pH (7 to 9) and a significant content of free carbonates (Gildersleeve and Ocampaugh, 1989).  When a plant that lacks certain metabolic abilities grows in calcareous soil, it develops symptoms of iron chlorosis that result because Fe isn't found in an available form.   The means used until now to solve the problem are:  local application of salts and chelates of Fe to the plants (application to soil or foliage), artificial modification of the pH of the soil solution (application of organic or inorganic acids) and use of cultivars with the ability to take Fe from soils where the element is unavailable. (Olsen et al., 1987; Chen y Barak, 1982; Emery, 1982).
 

2. PHYSIOLOGICAL IMPORTANCE OF IRON

In plants and other organisms a large part of the Fe present is found associated with porphyrins.  The Fe porphyrins of animals and fungi are principally heme molecules, while in plants the cytochromes are most common.  The cytochromes are found as functional parts of the respiratory and photosynthetic systems and their most important property, the redox function, derives from the capacity of Fe to oxidize reversibly from Fe(II) to Fe(III).  The capacity is used for rapid redox reactions for transferring electrons, that is, reactions that don't require transfering  H  or formation/destruction of covalent bonds.   The major part of Fe activity in plants is found in the redox reactions of the chloroplasts, mitochondria and [peroxisomas].  Iron is also implied in many enzymatic systems where it isn't associated with a prosthetic group or even associated structurally with the enzyme, although it plays a role thought to be important but poorly defined.  Table 1, modified from Rains (1976),  serves as summary:

Table 1.  Functional roles of iron.
 
1. Structural components of pophyrin molecules: cytochromes, heme, hematin, ferrichrome, animal and vegetable hemoglobins.  Involved in oxidation-reduction reactions in respiration and photosynthesis. 
2. Structural components of molecules without heme: ferridoxins and Fe-S proteins.
3.  Enzymatic systems: cytochrome oxidase, catalase, peroxidase, aconitase, fatty-acid desaturases, synthesis of chlorophyll (various enzymes), [peptidilprolina] hydrolase, nitrogenase, etc.

3. ABSORPTION AND ASSIMILATION OF IRON

Although Fe is the fourth most abundant element in the earth's crust, iron deficiency is a common problem for practically all species.  Fe is present in two oxidation states: Fe+3 (Ar3d5) or ferric and Fe+2 (Ar3d6) or ferrous.  In the presence of O2 Fe+2 is rapidly oxidized to Fe+3, which is poorly soluble in water and which precipitates as oxides of Fe.  For that reason, in our atmosphere rich in O2, the most thermodynamically stable form of iron is also the most difficult for organisms to access.  The question that arises is "How do biological organisms resolve the problem?"

The ions of heavy metals (such as Fe, Zn or Cu) don't freely cross the cell membrane.  The forms that pass are metal chelates.  The chelates are synthesized biologically and function to transport metal ions as so-called ionophores.  The ionophores specific to iron are known as siderophores (Emery, 1982; Olsen et al., 1981; Kloepper et al., 1980).  A general mechanism in the bacteria, cyanobacteria and fungi for the the transport of iron is excretion of siderophores into the growth medium and recovery of the same by a mechanism of adsorption, associated with the energy metabolism, which involves recognition on the part of the membrane receptor (Emery, 1982).  In many habitats and under many conditions there is competition for Fe among different organisms; the competition is decided by their relative ability to produce siderophores to complex iron (Emery, 1982; Olsen et al., 1981; Kloepper et al., 1980; Murphy et al., 1976).

3.1. Absorption of Iron by Ustilago sphaerogena and Other Microorganisms

The fungus Ustilago sphaerogena  was studied by J. Neilands in relation with iron metabolism starting in 1950 because, under normal conditions of Fe availability in the growth medium, the organism is capable of producing  up to 1% of its dry weight in the form of cytochrome c, a protein that contains iron.  In a study reported in 1952 (J. Am. Chem. Soc. 74:4846-4847) Neilands observed that under stress from iron deficiency the fungus excreted a large quantity of a substance that was crystallized, characterized and named ferrichrome by Neilands.  It was later shown that the siderophore ferrichrome had 3 hydroxylamine groups --CO--NOH--  which are known as potential chelating agents for Fe(III) (Emery, 1982).

The Fe transport system in U. sphaerogena is like that of many microorganisms (Figure 1).  When it detects an iron deficiency it induces a series of metabolic changes that translate to greater efficiency in the assimilation of that element.  Synthesis of cellular proteins diminishes and it channels its activity into production of deferriferrichromes (the organic part of ferrichrome) without iron.  The deferriferrichrome has an affinity constant for Fe of approximately 1029 (a value of 1015 or 1020 is considered very high) which why it can solubilize iron oxides.

Figure 1.  The Fe transport system of U. sphaerogena is typical of many microorganisms.  Ferrichrome is a cyclic hexapeptide that consists of three  parts glycine and three parts ornithine.  The terminal N of the ornithine is oxidized to hydroxylamine, -NOH-, and combined with three acetyl groups, CH3CO-, to give rise to the [hidroxamata] groups that complex Fe.  The deferri-ferrichromo shows great affinity for Fe(III), so rapidly forms ferrichrome+Fe(III) complexes.  This complex is carried into the cell by a transporter system and once in the interior the complex is reduced by siderophore reductase which causes liberation of Fe(II), forming new ferrichrome that is then excreted to the growth medium, reinitiating the cycle.
 

Ferric iron Fe(III) has three positive charges.  When Fe(III) is chelated by ferrichrome each hydroxylamine group loses a proton and that results in an electrically neutral molecule.  At the same time, the ferrichrome changes its shape and takes a very regular globular form.   This implies that the membrane receptor/carrier distinguishes betweem ferrichrome that carries Fe and that which doesn't.  Once in the interior of the cell, the Fe(III) is reduced to Fe(II) , using NADPH or NADH, by enzymes called siderophore reductases.  The affinity constant of ferrichrome for Fe(II) is very small so the Fe(II) is immediately freed from the ring chelant and channeled to the synthesis of a heme group. Once free of iron the deferri-ferrichrome is excreted back to the environment to initiate a new cycle (Emery, 1982).  Like U. sphaerogena the fungus Ustilago maydis produces a siderophore called ferrichrome that complexes Fe(III), this Fe-ferrichrome is adsorbed and in the interior of the cell the Fe(III) is reduced to Fe(II).  Moreover, of this activity Ardon et al. (1998) demonstrated that Ustilago maydis is capable of reducing Fe(III) complexes from non-native siderophores (xenosiderophores).  Unlike what happens with ferrichrome the authors found that the reduction is associated with the membrane and doesn't involve transferring the xenosiderophore into the cell.

In some organisms the iron-free siderophores are not recycled, instead the compound is hydrolyzed and a molecule of ligand is synthesized for every atom of Fe that is incorporated.  That is the case observed in Escherichia coli and Fusarium roseum (Emery, 1982).

3.2.  Absorption of Iron by Plants

The normal content of Fe in the tissue of vegetable crops is 50-300 mg kg-1 (ppm) in dry material (Zuang, 1982).  Olsen et al. (1981) mentions that, in general, the content of iron required for a typical crop during the growing season is 5-10 kg ha-1.  The content of Fe(III) in many soils is much higher than this level although, as was mentioned, the problem with this ionic form is its low solubility (Chen y Barak, 1982, Olsen et al., 1981).  In the aqueous soil solution the minimum concentration reported for reasonable growth in different crops is 10-9 molar.  Under standard conditions with pH=7 the concentration of Fe derived from Fe(OH)3 is 2x10-18 molar (see panel 1).  So then, plants must unavoidably have means to solubilize Fe(III)  from the oxides and hydroxides of iron.

Panel 1.  Effects of pH on the solubility of Fe(III).

Fe(OH)3 <-> Fe+3 + 3OH-

The solubility constant is: ksp = 2 x 10-39 = [Fe+3][OH-]3

Therefore: [Fe+3] = (2 x 10-39) [OH-]-3

if the pH = 7 then [OH-] = 10-7 and [Fe+3] = 2 x 10-18 M

if the pH = 9 then [OH-] = 10-5 and [Fe+3] = 2 x 10-24 M

if the pH = 6 then [OH-] = 10-8 and [Fe+3] = 2 x 10-15 M

if the pH = 4 then [OH-] = 10-10 and [Fe+3] = 2 x 10-9 M

Plants have two different ways or strategies that they use to improve the availability of Fe(III) in aqueous soil solution:

(i) Strategy I.  The monocotylodans except grasses and the dicotylodans can lower the pH in their rhizosphere.  Lowering the pH solubilizes Fe(III) and promotes it's reduction to Fe(II).  The solubilized Fe(III) is reduced to Fe(II) before it crosses the cellular membrane by the action of reducing proteins associated with the cellular membranes.

(ii) Strategy II.  Grasses excrete phytosiderophores, non-protein amino acids that solubilize Fe+3 ions and form an Fe-phytosiderophore complex (strategy II).  The release of phytosiderophores is positively correlated with genotypical differences in resistance to iron chlorosis.  Phytosiderophores also transport other cations such as Zn, Mn and Cu.

Strategy I plants use non-protein amino acids like nicotinamide for internal transport of Fe (that is to say, intra and intercellular).  A lack of nicotinamide causes  a shortage of iron in tissues.  That was observed in the cloronerva mutant of tomato (Lycopersicon esculentum) that has a fault in the gene that controls synthesis of the compound (Ling et al., 1996).  The phytosiderophores of the grasses have chemical structures very similar to nicotinamide (Figure 2).  Since methionine is the the precusor and nicotinamide an intermediary in the synthesis (Romheld, 1991),  it might be said that strategy II is an extracellular extension of the intra and intercellular Fe transport mechanism.

In strategy I pH is lowered by the excretion of protons (provided by an ATPase associated with the plasma membrane) and, in small measure, by a complex organic acid mixture, mainly citric and malic, which can function as chelating agents for iron and as a source of carbon for microorganisms.   Assumably the greater respiratory activity of the microorganisms associated with the rhizosphere reduces the level of O2 and generates microenvironments that facilitate the reduction of Fe(III).  The production and accumulation of citrate and malate in the roots induces greater PEPcarboxylase activity in the roots.  In the case of strategy II grasses there is production of organic acids but apparently no excretion of protons (Bienfait, 1988).

Figure 2.  Chemical structure of nicotinamide (top) and [mugineico] acid (bottom).

In some plants the initial response to an iron deficiency is the formation of transfer cells on the epidermis of the roots.  The cells release H+ ions, moreover they are the interface where the reduction of Fe(III) is carried out .  In the reverse case with available Fe in the substrate the transfer cells reduce their activity and die or disappear. (Brown and Jolley, 1989).  According to the results of Moog et al. (1995) induction of the transfer cells, as a response to an Fe shortage, can occur independent of an increase in the Fe(III) reduction activity.  This fact seems to indicate that the morphological and physiological responses to Fe are controlled by separate means.

Reduction of Fe(III) complexed with the chelate requires a transfer of electrons (e-) from the citosol across the plasma membrane.  The cells of strategy II plants have two e- transfer systems, a "standard" system present in all of the cells and a "turbo" or high high efficiency system (Figure 3),  that reduces distinct Fe-chelate complexes.  The "turbo" system is induced specifically in the epidermic cells of the roots by the absence of Fe.  Apparently the potential of the turbo reducing system comes from NADPH produced in the cytosol from NADP+-isocitrate dihydrogenase.  Isocitrate is formed from citrate by the mitochondrial aconitase enzyme (Bienfait, 1988).  The turbo system includes the Fe-chelate reductase enzyme (FCR) that is used by the majority of  plants (except grasses that lack the turbo system) for aquiring soluble Fe.  FCR is not apparently used for absorption of other cations such as Zn and Mn (Yi and Guerinot, 1996).  According to Moog et al. (1995) the FCR enzyme is induced by iron deficiency and follows Michaelis-Menten kinetics with Km of 45 uMol Fe(III)-EDTA and a Vmax of 42 nMol Fe+2 g-1 min-l.  Given the potential importance of FCR for engineering plants, there is a search for the genes responsible for coding the Fe-chelate reductase.  Robinson et al. (1999) isolated a gene called FRO2 that expresses Fe deficiency in roots of Arabidobsis thaliana.  The FRO2 gene seems to correspond to an Fe-chelate reductase and belongs to a genic superfamily of flavocytochromes that transport electrons through membranes.  According to the authors the isolation of FRO2 has implications for the generation of crops with greater nutritional quality and better growth in soils with low Fe content.

Figure 3.  The turbo system for transferring electrons associated with the plasma membrane of strategy I plants.
 

Fe(II) can be adsorbed by strategy I plants in complexed form with low-molecular weight ligands or in the free ionic form, the latter apparently being the more common.  In Arabidopsis thaliana the protein IRT1 (iron-regulated tranporter) is apparently a membrane-associated transporter of Fe(II) in free ionic form.  IRT1 is expressed in the roots, its synthesis is induced by Fe deficiency and its activity is inhibited by Cadmium (Eide et al, 1996).  In strategy II plants the Fe-phytosiderophore complexes, which are in high concentration (1 to 2 mMol) around the roots, are carried from the outside toward the interior of the cell by a high-affinity protein transporter.  As was mentioned, the phytosiderophores can work as transporters of other cations like Zn, Mn and Cu, but the high-affinity transport system is induced exclusively for Fe (Romheld, 1991).

Once it is absorbed by the roots, Fe(II) is first incorporated in ferritins -- iron-storage proteins that accumulate in the plastids of leaves and seeds.  (Clarkson and Hanson, 1980; Caris et al., 1995).  Fe is freed from ferritins by the reducing action of ascorbate (Laulhere and Briat, 1993) or phenolic reducers like caffeic acid, chlorogenic [ed. from "clorogenico"] acid, dihydrocaffeic acid and 3,4-dihydroxibenzoic acid.  According to the results of Boyer et al. (1988) the remobilization rate of Fe from ferritins depends on the concentration of phenolics and on their reducing power.  The authors observed that the enzymes and scavengers like catalase, the superoxide dismutase and manitol did not effect the rate of Fe removal.  To the contrary, EDTA and oxalate inhibit liberation of Fe.

Ferritins are proteins with similar structure in both plants and animals but with differing cytological locations and differing response to an excess of Fe.  The ferritins of plants are exported to the plastids and are regulated transcriptionally in response to a shortage of Fe.  The ferritins of animals are in the cytoplasm and their expression is regulated mainly by the level of translation of stored mRNA.  Another important difference is that the animals synthesize various types of ferritins depending on whether the ferritin will be used for storing Fe or for detoxifying the cells in case of Fe excess.  However, plants seem to show only one type of ferritin and in Arabidopsis thaliana it does not detoxify excess Fe.  This was the conclusion of Lescure et al. (1991) who considered that vacuoles possess great capacity to store Fe and that the constitutive ferritins of plants are not different from the ferritins induced by excess Fe (contrary to the case observed in animals). According to the authors, it is improbable that rapid synthesis of ferritins consitute a response to an excess of Fe.  Nevertheless the results of Becker et al. (1998), based on mutants of pea (Pisum sativum) with defects in the regulation of the adsorption of iron, show that plants accumulate Fe in ferritins and precipitate iron in deposits formed in the cytoplasm, mitochondrias and endoplasmic reticulum.  The authors' conclusion was that the observed response was a defense mechanism against accumulation of excesses soluble Fe, which causes oxidative stress.   The same conclusion was obtained by Deak et al. (1999) who worked with transgenic tobacco plants that synthesized alfalfa ferritins.  The transgenic tobacco retained normal photosynthetic function in the presence of toxicity caused by free radicals generated by excess of Fe or treatment with paraquat.   Additionally the offspring of transgenic plants that accumulate foliar ferritins exhibit tolerance to necrotic damage caused by viral pathogens (tobacco necrosis virus) and fungus (Alternaria alternata and Botryitis cinerea).  Apparently the intercellular capture of Fe by the ferritins protect plants from oxidative damage unduced by various types of stress.

At the release by the ferritins of the Fe(II) radical the iron moves to the remaining parts of the plant via the xylem where it again takes the form of Fe(III).  The average pH of the xylem exudate of different species is 5.5, which tends to turn Fe(II) to Fe(III).  The latter is transported to the areal parts of the plant as ferric citrate.  There is evidence indicating that before incorporating iron into ferritins in the leaves or seeds, Fe(III) together with the citrate must be reduced again to Fe(II) (Laulhere and Briat, 1993).  Apparently this reduction of Fe(III) to Fe(II) is a photochemical reaction induced by light in the blue-utraviolet range (Emery, 1982).

Lobreaux et al. (1992) determined that in corn (Zea mays) the presence of Fe (575 x 10-6 Mol) in seedlings exposed to a shortage of Fe induced rapid and abundant accumulation (24 hours) as soon as the ferritin mRNA appeared in the leaves.  The level of ferritin mRNA in the roots was stimulated by addition of iron.  The authors found that Fe accumulated in the roots was in the apoplastic fraction.  On the other hand, Lobreaux et al. (1993) found that in the case of plants the ferritins, in addition to being induced by Fe, responded to the application of exogenous abcisic [?] acid (ABA) , generating a transitory change in the ferritin mRNA.  Induction of the ferritin mRNA is very low in the mutant vp2 of corn that shows ABA deficiency.  The authors conclude that ABA is involved in the response of plants to Fe.  Finally, the report of Van Wuytswinkel et al. (1999) illustrates the importance of regulation of the concentration of ferritins.  In this work they obtained transgenic tobacco plants (Nicotiana tabacum) with overaccumulation of foliar ferritins that gave rise to an induced deficiency of Fe in the tissues.  This deficiency as well gave rise to the induction of Fe-reductase activity in the roots.  As follows from the previous paragraphs it seems that overexpression of ferritin diminshes the oxidative stress caused by Fe, but overexpression beyond a certain level gives rise to a deficiency of Fe.

The ferritins are of interest in studies to improve and genetically engineer the supply of Fe to the human population.  According to Theil et al. (1997) the selection of genotypes with greater content of ferritin in the seeds can be a viable strategy to increase the concentration of bioavailable Fe in the diet.

3.3. Role of Iron in Oxidative Stress

Like other transition metals, Fe can cause oxidative stress.  Oxidative stress is defined as the oxidative destruction of proteins, DNA, esters and unsaturated lipids of the membranes by the reactive metabolites of oxygen (like the superoxide anion, O2-, and hydrogen peroxide, H2O2) generated in endogenous processes.  Oxidative stress is controlled by the levels of reducing compounds like the [glutation] thiols and cistine as well as by the activity of scavengers like superoxide dismutase and catalase.   In agreement with Aust (1989) the peroxidation of lipids requires Fe(III) or Fe(II) probably in the form of O2-Fe complexes.  By itself Fe is capable of catalyzing redox reactions between oxygen and biomacromolecules, reactions that would not occur in the absence of Fe.  On the other hand, it is understood that iron complexes with ADP, histidine, EDTA, citrate and other chelating agents can facilitate the formation of reactive oxygen species that are capable of oxidizing thiols and that cause destruction of lipids by peroxidation.

Vansuyt et al. (1997) demonstrated that overfertilization with Fe in seedlings of Brassica napus caused rapid accumulation of ascorbate peroxidase mRNA, a scavenger for H2O2.  This was in addition to the ascorbate peroxidase expression induced by Fe and was independent of the response of the plant to other agents that cause oxidative damage.  That seems to indicate the existence of multiple responses to oxidative stress.  In the aquatic plant Hydrilla verticillata the application of FeCl3 was equivalent to the application of other oxidizing agents (Sinha et al., 1997), in that Fe generates peroxidative damage of lipids,  loss of K+ to the external medium (suggesting damage of the membranes), diminusion of the reduced form of [glutation] and increase of the oxidized form, increase in the activity of superoxide dismutase and diminution of the chlorophyll content.  The investigators' results indicate that the oxidative effect of Fe was related to the oxidation of thioles and with the generation of reactive species of oxygen.

Analogously, Caro and Puntarulo (1996) observed that the addition of Fe-EDTA in vivo up to an exogenous concentration of 5 x 10-4 M (that is to say, 500,000 times the minimum of 10-9 M), gives rise to an increase in the Fe content of the tissues accompanied by oxidative stress in the roots of soy (Glycine max).  At the subcellular level, the authors found that the Fe content and the rate of reduction of Fe-EDTA increased in isolated microbodies of the roots exposed to Fe when compared to a control without addition of Fe.  When compared to this control, the microbodies of the endoplasmic reticulum of the roots in the medium with iron showed a 55% increase in generation of the superoxide anion, and as much as four times the rate of production of hydroxide radicals.  On the other hand the supplementation of Fe did not affect the activity of antioxidant enzymes nor the total content of thiols,  although the alpha-tocopherol content diminished significantly.  In this respect the report by Caris et al. (1995) is interesting.   They indicate that Fe chelated with a synthetic siderophore (O-Trensox) did not generate oxidative damage, as occured with Fe-EDTA and Fe-citrato.

3.4. Absorption of Iron by [Diazotrofos] Nitrogen-Fixing Symbionts

Literally diazotrofo means "dining room of nitrogen or N2", and refers to the well-known capacity of legumes to associate with bacterias of the genus Rhizobium and Bradyrhyzobium forming symbiotic tissues with the capacity to reduce N2 to NH3.  A deficiency of Fe can limit the symbiotic fixation of N2, modify the survival and growth of the rhizobia in the soil and restrict the initiation and development of the nodules until it damages the nodule function and growth of the plant.  Extensive variation in the ability to  survive and to grow under stress of Fe deficiency has been detected as much in the symbiotic bacteria as in host plants.  It's understood for example that different Bradyrhizobium stocks have different capacity to excrete siderophores, and that these differences seem related to the ability of the bacteria to nodulate roots in calcareous soils (Tang, et al., 1992).

In the absence of Fe, faults appear in nodulation related to scant growth and liberation of [the effected bacteria].  The final result is growth restriction of nodule meristems and the absence of nodule function (Tang et al.,1992).  In Rhizobium leguminosarum a shortage of Fe causes reduced levels of cytochromes b and c as well as an accumulation of porphyrins (precursors of heme groups), that are detected by red-pink fluorescence when the colonies are illuminated with UV light.  On the other hand, some mutants such as Rhizobium leguminosarum 116, with very low capacity for assimilation of Fe, give small white nodules but without obvious micromorphological abnormalities in the nodule [formed by Fe-deficient bacteria](Nadler et al., 1990).

In the case of legumes the management and production of new cultivars for calcareous soils requires an integral approach that takes into account the presence of the legume-bacterial symbiont system (Tan et al., 1992).

3.5 Competition for Iron in the Rhizosphere and Phytopathogens

Application of certain bacteria intended to suppress diseases caused by soil pathogens may translate to greater growth and yield by plants.  The mechanisms of antagonism are competition, parasitism, predation and antibiosis.  In the case of certain rhizobacteria (bacteria associated with the roots), such as Pseudomonas, the ability to complex Fe with siderophores is the key mechanism for supressing pathogens.  Nevertheless this is far from being a demonstrated fact (Alabouvette et al., 1996) and to the contrary the production of antibiotics and growth inhibitors can be more important as a suppresive factor (Gill and Warren, 1988).

3.6 Physiological Consequences of Iron Deficiency

The most obvious symptom of an iron deficiency is foliar iron chlorosis.  Iron chlorosis is a complex physiological disorder.  At least 10 different causes are known to induce iron chlorosis and, when observed, it is commonly caused by at least two of them in conjunction (Peterson and Onken, 1992).  The final phase of iron chlorosis, with extreme deficiency of Fe, is usually necrosis and death of the leaves.  Great dysfunction in the photosynthetic apparatus is observed before this occurs.  Winder and Nishio (1995) determined that the RUBISCO content and RUBISCO CO2 fixation activity are diminished by 60% and 66%, respectively in leaves with severe Fe stress.  The RUBISCO content was dependent on the availability of mRNAs and as much this drop in the amount of polypeptides as the fall in the CO2 fixation activity is correlated directly with the chlorophyll content.  On the other hand the activation of RUBISCO by the RUBISCO activase was also reduced by 27% in stressed leaves.

In the cyanobacteria Oscillatoria tenuis it's observed that, within the range of Fe concentrations from 4.2 x 10-5 to 5.1 x 10-9, the rate of growth isn't limited by the photosynthetic capacity but by another undetermined cellular functions.  Also the deficiency of Fe in the growth medium induced the synthesis of extracellular siderophores and of specific proteins whose function is probably related to the transport of Fe to the interior of the cell.  This activity was correlated with the recovery of growth in cells in media poor in Fe.   Nevertheless, in spite of the activation of this high affinity transport system the rate of growth didn't increase to the levels observed in a media with an adequate level of Fe (Trick et  al., 1995).
 

4. INTER- AND INTRASPECIFIC DIFFERENCES IN THE ABILITY TO ASSIMILATE IRON

The ability of a plant or other organism to assimilate iron depends on the conjunctive action of a series of mechanisms that were analysed briefly in previous paragraphs.  This ability or efficiency is rather variable between species and between cultivars,  stocks or varieties within the same species (Bianfait, 1988).  As an example, Brown and Olsen (1980, J. Plant Nutrition 2:661-682) found that dicotylodons were in general more efficient at handling an iron deficiency than the monocotylodons.  In the same way, there are differences detected between cultivars of species of crops like soya, bean, tomato, sunflower, corn, barley, sorghum, etc.  Between the grasses that use strategy II there are species resistent to iron chlorosis (like wheat, barley and rye) and species susceptible to this problem (like sorghum).  It has been demonstrated that the difference in efficiency depends on the amount of phytosiderphores excreted to the  rhizosphere combined with the action of other alternative mechanisms for the absorption of Fe like the capacity to absorb the siderophores of microbes and induction of a Fe+3 reductase for the passive adsorption of iron chelates (Romheld, 1991).

Rodriguez de Cianzio (1991) mentions that although iron chlorosis is an extensive problem, genetic improvement aimed at this characteristic have been made in a few species like oats (Avena byzantina), sorghum (Sorghum bicolor), beans (Phaseolus vulgaris), soy (G. max), peanut (Arachis hypogea), clovers (Trifolium spp.), forage grass (Botriochloa sp.), chile (Capsicum annuum), citruses (Citrus sp.), mango (Mangifera indica) and avocado (Persea americana).

In that respect Ambler et al. (1971) found differences in the ability to reduce Fe(III)  to Fe(II) between two cultivars of soy and classified one as efficient and the other as inefficient at assimilating iron.  Gildersleene et al. (1989) detected great variability in the response to Fe deficiency in 22 cultivars of clover from three species.

Also, Fehr's group at the University of Iowa developed a program of recurrent selection for obtaining cultivars of soy with efficiency in absorption and assimilation of iron in calcareous soils.  The result at mid-term was a population called AP9 that is the source for lines that show good performance in state and national tests by the University of Iowa and USDA (Rodriguez de Cianzio and Fehr, 1982; Beeghly and Fehr, 1980; Dranonuk et al., 1989; Diers et al., 1991).

Selection of progenitors and lineages with improved resistance to iron chlorosis requires correct identification of superior genotypes.  Different methods were used successfully for characterizing resistance to iron chlorosis:  visual indices, foliar content of chlorophyll and the ability to excrete reducing compounds from the roots.  In particular visual indices that correlated with the foliar content of chlorophyll were useful and practical results (Peterson and Onken, 1992).

Some plants used traditionally in treatment of anemia show very high levels of Fe in their tissues, e.g. Bridelia cathartica with 356.9 ppm Fe and Lannea stuhlmannii with 352.1 ppm, both plants of the African continent (Omolo et al., 1997).  Probably study of the mechanisms of absorption and accumulation of Fe by these and similar plants can shed more light on the genetic mechanisms and physiological implications.  Also, more study is needed to clarify if genotypes resistant to iron chlorosis assure that we will be able to rely on crops of better nutritional quality with an adequate level of bioavailable Fe.
 

5. CORRECTION OF AN IRON DEFICIENCY

A value for available Fe of less than 11 ppm in soil is considered low.  Optimum values are between 12 and 24 ppm and the management of the soils and fertilization is intended to obtain and maintan these values because normally there is a correlation between the Fe available in the soil and that observed in vegetables.

Organic matter in the soil exerts a positive effect on the solubility of iron through a reductive effect out of proportion with the amount of Fe contained in the biomass.  It is known for example that adding organic matter to a soil deficient in available Fe exerts a positive effect on the plants, but on the other hand the same response is not observed from adding ashes originating from the same amount of organic matter. Biological degradation of the organic matter contributes e- and other reducing agents that lower the redox potential of the soil, creating reducing microenvironments (deficient in O2) in the soil where the concentration of Fe(II) available to the plants is increased.  It follows from this that application and maintenance of organic matter in the soil translates to adequate long term availability of iron (Lindsay, 1991).

An adequate supply of potassium is related to a better response to iron deficiency, as much in plants that use strategy I as in those that use strategy II (Huges et al., 1992).

Briefly the ways to correct an iron deficiency are (Zuang, 1982; Morard, s.a.):

- Application of iron chelates (EDTA, DTPA, HEDTA or EDDHA) to soils or to the foliage, for annual crops applications to soils are expensive and ineffective.

- Application of iron salts (such as iron sulfate) to soil or to the foliage, for annual crops the application to soils are expensive and ineffective.

- Application of phosphoric acid, sulfuric acid or nitric acid (or KOH if the soil is acidic) in irrigation water to modify the soil solution.  The recommended dosage varies according to the situation, but the application of 10 or 20 liters per hectare is common in production systems with drip irrigation.

Alternatively one can do the following:

- Application to the soil of 60-200 kg of agricultural sulfur or 10-15 kg of iron sulfate heptahydrate (20% Fe) per hectare, incorporated with a harrow.  This application can be localized only in the seed bed; in that case use 40-80 kg of sulfur and 3-5 kg of iron sulfate per hectare and incorporate it with a rototiller.  The acidification effect of sulfur and sulfate facilitate the absorption of Fe by plants.

- Application of ammonium sulfate (300-500 kg per hectare or 30-50 g per m2) dissolved in water for fertilized irrigation or applied superficially and later incorporated with a machine.

Panel 2 (Zuang, 1982) presents information about conditions for application of iron chelates used in agriculture:
 

Panel 2. Basic information about iron chelates.
 
CHELATE 
Fe CONTENT 
RANGE OF CONDITIONS FOR USE 
EDDHA 
5.9 to 7 % 
soil pH 3 to 9; no exposure to ultraviolet radiation 
HEDTA 
2 % 
soil pH  3 to 7.8 
DTPA 
2.0 to 2.2 % 
soil pH 3 to 7 
EDTA 
1.8 to 2.3 % 
soil pH 3 to 6.5 

A nutritive solution applied to the foliage must contain between 0.6 and 1.5 mg/l (ppm) of Fe, that is to say, 0.06 to 0.15 g of Fe for each 0.1 m3 or 1.07 x 10-5 to 2.69 x 10-5 molar of Fe.  This dose can be duplicated in case symptoms of chlorosis reappear.  For soil application the normal dosage is 20 to 25 kg of commercial product per hectare (from 300 to 3000 g Fe per hectare).  In golf courses Glinski et al. (1992) applied 1.12 kg Fe per hectare every 30 days in the form of Sequestrene 330 (DTPA).

To apply commercial produces that have various microelements incorporated in their formula the dosage of Fe (average for horticultural crops) are as follows:
 
PRODUCT NAME 
Fe CONTENT 
FOLIAR DOSAGE 
SOIL DOSAGE 
Fertiquel-Combi (BASF) 
5 % 
0.5 - 1.5 kg/ha 
3 - 10 g/m2
Poliquel Fierro (GBM) 
8 % 
2 - 3 liters/ha 
 
Foltrón plus (GBM) 
500 ppm 
2 - 3 liters/ha 
 
Mastergrow (Mastergrow International) 
0.10 % 
0.5 kg/ha 
 

Karkosh et al. (1988) made applications of Sequestrene 138 Fe (Fe-EDDHA) to seeds (applying 10 g of Fe-EDDHA plus 5 g of Biosorb* per kg of seed) of soy cultivares with different Fe adsorption efficiencies.  The treated seeds were planted in calcareous soils with pH=8.0.  The authors found that the application significantly improved the yield of efficient cultivars but did not help in the case of the inefficient ones.

*Biosorb (Energro, Inc.) is a hydrophilic starch based polymer with which the seeds were covered.
 

6. BIOAVAILABILITY OF Fe

According to Gibson (1997) the most effective technological strategies to combat iron deficiency in the less industrialized countries include various tactics: (i) supplementing Fe for high risk groups, (ii) promoting among high risk groups the use of fortified food such as diets designed to maximize the bioavailability of Fe and (iii) maximizing  the bioavailability of Fe intrisic in the animal and vegetable foods.  In the case of the vegetables, intrinsic Fe is that which is accumulated in the tissues from the soil or from foliar fertilization and can be increased by agricultural management.

High concentrations of Fe in vegetables does not imply necessarily that the iron is available when consumed.  Deficiency of iron in humans is partially produced by ingesting diets that contain low levels of bioavailable Fe, by the action of inhibitors like tannins or phytate,  by low levels of promotors or by low levels per se of iron (Gibson, 1996).  He calls bioavailability the fraction of content of an element that is really usable by organisms that consume the vegetable.  Bioavailability can be modified by a multitude of genetic and environmental factors.  In that respect Reddy et al. (1993) demonstrated that there is a direct relation between the content of available Fe in soil and the concentration of Fe in the tissues of spinach (Spinacea oleracea), but that high concentration of Fe did not imply high bioavailability and the Fe.  Considering the forgoing data it is obvious that there is a great opportunity in the development and optimization of pre and postharvest technologies that allow development of grains, seeds, fruits and vegetables with superior nutritional quality.
 

7. CONCLUSIONS

Regulation and control of the capture-assimilation-accumulation of Fe on the part of plants is very complex, involving different mechanisms that much improve the solubilization and absorption of said element.  These processes were reviewed in a summary manner but it is clear that there are large reservoirs of knowledge of these processes.  Fe deficiency is a very extensive problem that can be alleviated in part by improving the proportion of this element in the vegetables, seeds, fruits and grains that the population consumes.  Multiple major studies aimed to avoid and correct iron chlorosis are necessary mainly for the regions where the availability of Fe in soils is low.  The studies must also consider the bioavailability of Fe as an integral part of programs to manage and optimize the technology.  Although short term, the administration of dietary suppliments and the fortification of foods results in an increase of Fe in the population that consumes it; in reality only certain sectors of the population see benefits.  Long term, a suitable contribution of Fe for all the human population will arise from a greater understanding of natural mechanisms for solving the problem.
 

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