Plant Metabolic Responses to Iron-Deficiency Stress

Plant Metabolic Responses to Iron-Deficiency StressAuthor(s): John C. Brown and Von D. JolleySource: BioScience, Vol. 39, No. 8 (Sep., 1989), pp. 546-551Published by: University of California Press on behalf of the American Institute of Biological SciencesStable URL: http://www.jstor.org/stable/1310977 .

Accessed: 04/10/2013 05:39

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

University of California Press and American Institute of Biological Sciences are collaborating with JSTOR todigitize, preserve and extend access to BioScience.

http://www.jstor.org

This content downloaded from 192.236.36.29 on Fri, 4 Oct 2013 05:39:26 AMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=ucal

http://www.jstor.org/action/showPublisher?publisherCode=aibs

http://www.jstor.org/stable/1310977?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


Plant Metabolic Responses to

Iron-deficiency Stress A variety of mechanisms, grouped into two major strategies,

make iron available from the soil

John C. Brown and Von D. Jolley

germinating soybean seed contains sufficient iron to supply the plant until the first

trifoliate leaf is produced. If a contin- uous supply of iron from the growth medium is not then available, the plant develops iron chlorosis-a yel- lowing that can be alleviated by sup- plying the plant with suitable iron compounds. This disorder is particu- larly prevalent on calcareous soils, found on approximately one-third of the earth's surface. In these soils, it is difficult to maintain iron in forms that are usable by plants.

Iron per se is seldom deficient in soils, being the fourth most abundant element in the earth's crust (Kraus- kopf 1972). It exists in two valency states, ferric (Fe3+) and ferrous (Fe2+), and it is active in oxidation/ reduction reactions in both soils and plants. Plants are better able to take up and use ferrous iron than ferric iron. But under the usually prevailing conditions in soils and biological fluids, iron is predominantly in the ferric state. The soil pH also strongly influences iron solubility and therefore availability to plants. For example, for each pH unit increase above 4.0, the solubility of iron decreases by

Biologists are challenged to select for iron efficiency in plants

a factor of approximately 1000 (La- timer 1952).

Despite the low solubility and the- oretically insufficient level of available iron in calcareous soils, many plants grow well there. They do so because plants have a strong influence on the rhizosphere and ultimately control the solubility of iron and its availability to plants (Lindsay and Schwab 1982). Some plants can reduce ferric to ferrous iron at their roots. Many plant roots can also release hydrogen ions to acidify the soil or can release chelating agents to make the iron in the soil more available. These plant responses to iron- deficiency stress have developed through genetic adaptations to the prevailing conditions in various habi- tats (Bjorkman and Berry 1973).

In recent years, scientists better un- derstand the adaptive mechanisms for making iron available to plants. Many scientists worldwide have con- tributed to this understanding; in this article we illustrate current concepts with examples primarily from our research.

Genetic mechanisms of the roots

Response to iron-deficiency stress is adaptive and is known to be geneti-

cally controlled in several plant species (Bell et al. 1958, Wann and Hills 1973, Weiss 1943). Plants have specific iron requirements dependent on their ability to make iron available in a usable form. Weiss (1943) showed that PI-549-19-5-1 (now T203 soybean [Glycine max L.]) was very sus- ceptible to iron-deficiency stress, whereas Hawkeye (HA) soybean was not, and he termed T203 soybean iron inefficient and HA soybean iron efficient.

Brown et al. (1958) grafted iron- inefficient T203 soybean tops on iron- efficient HA rootstock and iron- efficient HA tops on iron-inefficient T203 rootstocks. The iron-inefficient plants grafted on the iron-efficient rootstock became iron efficient and remained green. The iron-efficient plants grafted to iron-inefficient rootstocks became iron-inefficient, the new developing leaves turned yellow, and eventually the plant died.

This reciprocal graft experiment was repeated using T3238fer (iron- inefficient) and T3238FER (iron- efficient) tomato (Brown et al. 1971) with similar results. Thus, it was es- tablished that the controlling factors in absorption and transport of iron are located in the root. Figure 1 shows how these two tomato (Lyco- persicon esculentum Mill.) cultivars responded when grown on a calcareous soil; T3238fer was chlorotic, whereas T3238FER was green. Brown (1961) concluded that the iron-efficient plants must initiate some metabolic process that affects the solubility or availability of iron at the roots. Nutrient solutions were

John C. Brown was formerly a research scientist at the Plant Stress Laboratory, Plant Physiology Institute, BARC-USDA, Beltsville, MD 20705 and is currently an adjunct professor of agronomy at Brigham Young University. Von D. Jolley is an associate professor of agronomy in the Department of Agronomy and Horti- culture, Brigham Young University, Provo, UT 84602. ? 1989 American In- stitute of Biological Sciences.

546 BioScience Vol. 39 No. 8



used in subsequent experiments to determine those factors.

Using nutrient solutions, reductive capacity of the roots of iron-stressed HA and T203 soybeans was determined using a ferricyanide-ferrichlo- ride solution as a source of ferric iron (Brown et al. 1961). The blue color that developed on HA roots was in- dicative of Fe3+ reduction to Fe2+ by the roots. Prussian blue (ferric ferro- cyanide, Fe4[Fe(CN)6]3) was visually present on the lateral roots of HA soybeans after 6 hours. The lack of blue color development in the iron- inefficient T203 soybean roots suggested that they did not reduce Fe' to Fe2+. This result indicated a relationship between the reductive capacity of HA and T203 soybean roots and their ability to absorb iron from the growth medium.

This same relationship was ob- served in the iron-inefficient T3238fer and the iron-efficient T3238FER tomato. The latter released hydrogen ions from their roots concomitantly with reduction of Fe3+ to Fe2+ in response to iron-deficiency stress (Brown et al. 1971). Marschner et al. (1974) made similar observations using sunflower.

During the past 25 years, addi- tional research has characterized five types of responses to iron-deficiency stress in many different plant species or varieties within the species that make iron available for plant use. These factors are not common to all plants. One factor, release of chelators called phytosiderophores, have thus far been found only in barley (Hordeum vulgare L.) and oats (Avenae sativa L.). In some dicotyledonous plants, for example the tomato, soybean, and cotton (Gos- sipium hirsutum L.) plants that we have studied, the four other factors are all in evidence. In other dicots and monocots, two or three of the factors function to make iron usable by the plant. All the above factors enhance absorption of iron and its translocation to plant tops.

Marschner et al. (1986) categorized plants by their response to low iron availability: the first strategy is employed by all dicots and monocots with the exception of the grasses. The second strategy is used by grasses (graminaceous mononcot species). Below we give a brief description of

the factors used by plants in making iron available in response to iron- deficiency stress.

Iron-chelating substances released by roots The release of natural iron-chelating substances (phytosiderophores) is the most recent plant response to iron stress to be discovered. It has been reported in barley and oats (Marsch- ner et al. 1986, Mino et al. 1983, Romheld and Marschner 1986, Tak- agi 1976, and Takagi et al. 1984). So far there has been no report of a phytosiderophore released by any di- cotyledon in response to iron-deficiency stress.

Release of phytosiderophores is the primary response to iron-deficiency stress in barley and oats. Formation of Fe3+phytosiderophore solubilizes ferric iron in nutrient solutions and in soils. Mino et al. (1983) suggested that the mechanism for absorption and transport of iron in graminaceous plants involves the excretion of mugineic acid from the roots, which aids in Fe3+ solubilization and reduction of Fe3+ to Fe2+. Takagi et al. (1984) isolated mugineic acid from root washings of barley that enhanced iron solubility between pH 4.0 and 9.0. They were unable to isolate any mugineic acid-like chelators from dicotyledonous plants. They suggested that in graminaceous plants mugineic acid should be regarded as a phytosiderophore with physiological behavior

similar to the microbial siderophores described by Neilands (1981).

Romheld and Marschner (1986) suggested that mugineic acid released by barley roots in response to iron- deficiency stress is responsible for sol- ubilizing ferric hydroxide. Marschner et al. (1986, 1987) suggested that phytosiderophore release was associated with the apical root zones in grasses and that the Fe3+ was translocated across the plasma membrane without involvement of a reduction step (Fe3+ to Fe2+) by a membrane- bound reductase.

All the plants found to release the phytosiderophore are iron-efficient. In oats, McDaniel and Dunphy (1978) identified iron-efficient Coker 227 and iron-inefficient TAM 0-312 in the field. Jolley and Brown (in press) tested these two cultivars under iron-deficiency stress conditions in nutrient solutions. They found that Coker 227 oats released a phytosiderophore over a range of iron in the nutrient solution from 0.0 to 4.8 mg Fe/l (no synthetic chelate in solution). The TAM 0-312 oats did not release a phytosiderophore, and it was chlorotic in all of the treatments (Figure 2). Even with 2.4 mg Fe/l in the nutrient solution, Coker 227 released a phytosiderophore and developed iron chlorosis with time. It took 4.8 mg Fe/l in the nutrient solution for Coker 227 oats to remain green without the release of a phytosiderophore.

Another graminaceous plant that is iron-inefficient is

ysl corn (Zea mays

Figure 1. Chlorotic T3238fer (iron-inefficient; left) and green T3238FER (iron-efficient; right) tomatoes grown on a calcareous soil.

September 1989 547



9 6 COKER 227 TAM 0-312

5-

S 4- TAM 0-312 7 -c

S23- 6 - 2 COKER 227

51-

4. . . . . ..... 0 0 10 20 0 10 20

DAY DAY

3- 1 100

E 80 COKER 227

S2 COKER227 . 60

40-

S. 1TAM 0-312

20 TAM0-312

0 0 , 1

0 10 20 0 10 20

DAY DAY

Figure 2. Periodic measure of solution pH, chlorosis rating, ferric iron solubilized (phytosiderophore), and leaf iron concentration of TAM 0-312 and Coker 227 oats with 1.2 mg/l iron in solution.

L.; Bell et al. 1958). WF9 corn is considered iron efficient (Clark and Brown 1974). These two cultivars have been tested for release of a phytosiderophore in response to iron- deficiency stress, but neither of the cultivars released a phytosiderophore.1 Instead, WF9 corn released some hydrogen ions and the roots reduced some Fe3? to Fe2+, responses more typical of dicotyledonous plants. It appears that all graminaceous plants do not use the same strategy.

More work needs to be done in characterizing the phytosiderophore and its effect on iron absorption and transport. The phytosiderophore may act mainly to solubilize or chelate the iron in the growth medium, and reduction of Fe3+ to Fe2+ is necessary at the root for absorption/transloca-

tion of iron into the plant. For example, it has been found that growing Coker 227 with WF9 in nutrient solutions is beneficial to iron uptake by WF9 corn. The growth of

ysl and

Coker 227 in the same solutions did not make iron available to

ysl corn.2

When the iron is chelated, either by synthetic chelates or phytosiderophores, in a growth medium (soil or nutrient solution), it diffuses to the root, where it is reduced from Fe3+ to Fe2+ and absorbed by the root. The chelating agent may diffuse away to become resaturated with iron from the growth medium.

Release of hydrogen ions

Symptoms of iron chlorosis are avoided when hydrogen ions are released from roots and consequently

the pH of the nutrient solution de- clines. A lowering of the pH provides a more favorable environment for the reduction of Fe3+ to Fe2+ (Figure 3; Camp et al. 1987). Hydrogen ion release is found predominantly in dicotyledonous plants. Barley and oats release few hydrogen ions in response to iron-deficiency stress.

In some plants, the initial response to iron-deficiency stress is formation of transfer cells in the epidermis of the roots (Kramer et al. 1980). These cells release hydrogen ions and produce and release reductants, which enhance iron absorption/translocation within the plant. When iron is made available to the plant, the transfer cells lose activity and degenerate (Landsberg 1984).

The iron-inefficient T3238fer tomato does not develop transfer cells, whereas the iron-efficient T3238FER tomato does (Landsberg 1982). Con- sequently, the T3238fer tomato does not release hydrogen ions from its roots (Brown and Ambler 1974), whereas the T3238FER tomato causes a steep decrease in the pH of the nutrient solution in response to iron-deficiency stress. Some plants classed as iron-efficient do not develop transfer cells in response to iron-deficiency stress (Landsberg 1984), but instead prolific root hair formation is associated with hydrogen-ion release (Ambler et al. 1971).

Potassium appears to play a key and specific role in a plant's response to iron-deficiency stress. Iron-efficient tomato and soybeans do not release hydrogen if the plants are under both potassium- and iron-deficiency stress (Jolley and Brown 1985, Jolley et al. 1988), even though the plants developed iron chlorosis. Equimolar sodium or rubidium ions did not substi- tute for potassium in eliciting the release of hydrogen ions.

Release of reductants Reductants are released from roots of some dicotyledons in response to iron-deficiency stress (Brown et al. 1971, Landsberg 1984, Marschner et al. 1974). Reductants released into nutrient solution by iron-efficient tomato plants are effective in reducing Fe3 to Fe2+, but such release was not measurable on iron-inefficient plants. Olsen et al. (1981) found that caffeic

1V. D. Jolley and J. C. Brown. 1989. Unpub- lished data.

2V. D. Jolley, C. M. Lytle, and J. C. Brown. 1989. Unpublished data.




acid was the principal component of the reductant fraction in the exudate of iron-deficiency stressed, iron- efficient tomato roots.

Barrett-Leonard et al. (1983) and Sijmons and Bienfait (1984) proposed that the quantity of released reductants from roots is not sufficient to supply adequate ferrous iron to plants. They infer, therefore, that reductants are not an essential factor in making iron available to plants. But reductants may be concentrated in- side the root or at the root-soil inter- face maintaining iron in its more available ferrous form (Ambler et al. 1971). In this way, reductants may be important in making iron available for uptake or transport by the plant.

8

7- 0.75 mg/L Fe

6

5 0 mg/LFe

4

3 0 2 4 6 8 10 12

DAY 4

0 mg/L Fe

3

2

S10.75 mg/L Fe

0 '

0 2 4 6 8 10 12 DAY

+ 0.6 0 mg/L Fe

S0.5

E 0.4

g 0.3

S00.75 mg/L Fe 8 0.2

0.1

0.0 0 2 4 6 8 10 12

DAY

Figure 3. Fluctuations in pH, reductant, and root reduction of Fe3 + by A7 soybean in response to 0 and 0.75 mg/i iron with time. Differences between 0 and 0.75 mg/1 iron on a given day were significant at the 0.05 level on days 4-11 (pH), 6-11 (reductant), and 5-11 (root reduction). From Camp et al. 1987.

Reductants are not usually released from the root until the pH of the nutrient solution is pH 4.5 or lower. There is a concomitant relationship between hydrogen ion release, reductant release by roots, and Fe3+ reduced to Fe2+ by roots of iron- efficient soybeans and tomatoes (Figure 3; Camp et al. 1987).

Some plants seem to balance hydrogen-ion and reductant release. For example, muskmelon (Cucumis melo) exhibits enhanced reduction of Fe3+ to Fe2+ by roots, although no reductant is released.3 Excessive hydrogen- ion release appears to compensate for no reductant being released by the muskmelon plant.

Reduction of Fe3+ to Fe2+

Although other factors make iron sol- uble in the soil and available to the root, reduction of Fe3? to Fe2+ by the roots is the primary factor in making iron available for absorption. This reduction occurs in both dicots and monocots. Bienfait et al. (1982) sug- gest that Fe31 is reduced to Fe2+ at the plasma membrane by an enzy- matic process involving a reductase. Chaney et al. (1972) showed that for plants to use Fe3+ from several chelates in a nutrient solution, Fe3+ was reduced to Fe2+, which was taken up by the plant. As an example, when Fe3 EDDHA (ethylenediaminedi- [o-hydroxyphenylacetate]; stability constant of 33.9; Schroder 1964a) is reduced to Fe2+EDDHA (stability constant of 14.3; Schroder 1964b), iron becomes more available to the plant.

Tiffin et al. (1960) studied the absorption of Fe3+EDDHA by iron- efficient zinnia (Zinnia elegans Jacq.), sunflower, and soybean. They found that iron was released to the roots, but most of the EDDHA remained in the nutrient solution. Also, three chelating agents labeled with the radio- isotopes SSFe and 14C showed that iron-deficiency-stressed soybeans (which are iron efficient) translocated much more SSFe in their stem exudate than 14C; apparently the SSFe was separated from the chelating agent at the root (Tiffin and Brown 1961).

As with hydrogen-ion and reduc-

tant release, the young lateral roots were the principal sites of Fe3 reduction in both iron-efficient soybean (Ambler et al. 1971) and tomato (Brown and Ambler 1974). Most of the Fe31 was reduced to Fe2+ in areas of the root accessible to BPDS (bathophenanthrolinedisulfonate), a relatively strong chelator of Fe2+ (log K = 21.8; Brown and Ambler 1974). As the Fe3+ was reduced to Fe2+, most of it was trapped in the nutrient solution as Fe2+ (BPDS)3 and was not transported to plant tops (Brown and Chaney 1971).

Plants have the ability to maintain a reduced environment around roots (Lindsay and Schwab 1982). These reductive mechanisms may vary among plant species and varieties within species, but they play an important role in making iron available for absorption by the plant. Byers (1986) indicates that for a ferrous iron uptake system to function in an aerobic environment, the cells must be able to externally reduce ferric iron.

12

10 HA-Soybean 7

s

6

4

2

.-

PI-Soybean

o 0 2 4 6 8 10

X10-6 M FeEDDHA in Absorption Nutrient

S50

40 HA-Soybean ,, a 40

o

30

20

0-. M FPI-Soybean

0 2 4 6 8 10 X10-6 M FeEDDHA In Absorption Nutrient

Figure 4. Hawkeye (HA) and PI-54619- 5-1 (now T203) soybean under iron- deficiency stress, showing the absorption- translocation of iron and the concomitant translocation of citrate in the stem exudate as the iron concentration in the nutrient solution increases. Iron-inefficient PI soybean did not absorb and translocate iron or citrate (Brown and Tiffin 1965).

3V. D. Jolley, J. C. Brown, and P. E. Nugent. 1988. Unpublished data.

September 1989 549



Iron transported as iron citrate The xylem exudate of several mono- cot and dicot species has a pH of approximately 5.5, which would tend to convert Fe + to Fe3+. Tiffin (1966, 1972) electrophoretically identified Fe3+ citrate in the xylem exudate of several plant species and suggested that citrate is the natural carrier of iron in xylem transport. When iron- deficiency-stressed plants were placed in nutrient solutions containing various levels of iron, as iron was in- creased, there was a parallel increase in iron citrate in the xylem exudate (Figure 4; Brown and Tiffin 1965). In iron-efficient soybean and tomato, reduced iron appears to move through the protoxylem of the young lateral root to the metaxylem of the primary root, where it is oxidized to Fe3 , chelated by citrate, and transported to plant tops (Brown 1978).

In addition to serving as a trans- porting agent for iron, citrate appears to have a role in iron nutrition. It enhances reduction of Fe3+ in a photochemical reaction induced by sun- light (Frahn 1958) and by cool-white fluorescent light (Brown et al. 1979). Citrate also alleviated inhibitory effects of phosphate and pH (up to pH 6.0) on the reduction of Fe3+ to Fe+.

Response to the environment We can collectively term the factors that respond to iron-deficiency stress in plants as the iron-stress-response mechanism. When this mechanism is actively functioning, the rate of iron uptake by the plant markedly increases, but this response may be only temporary. As iron is made available to the plant and the chlorotic terminal leaves regreen, the functioning of the iron-stress-response mechanism decreases. The mechanism may be turned on again if iron-deficiency stress increases and more iron is needed by the plant (Brown 1978).

Although iron-efficient plants vary in which factors they display of those included in the iron-stress-response mechanism, they still obtain iron from the growth medium. For example, iron-efficient muskmelon prolifi- cally produces hydrogen ions and re- duces Fe3 to Fe2? at the roots to overcome iron-deficiency stress, but

does not release reductants from its roots.4

External factors known to affect the overall plant response to iron- deficiency stress are potassium-deficiency stress and the quality of light. In addition to retarding hydrogen-ion release, potassium stress also de- creased reductant release and the reduction of Fe3+ to Fe2+ by the roots. Substituting sodium or rubidium for potassium did not correct the condi- tion (Jolley and Brown 1985, Jolley et al. 1988).

Brown et al. (1979) and Olsen and Brown (1981) showed that cool white fluorescent light reduced Fe3+ to Fe2+, but low-pressure sodium light did not. Jolley et al. (1987) and Push- nik et al. (1987) showed that under both lighting conditions the iron- deficiency-stressed cotton plants released hydrogen ions from their roots. However, despite the release of hydrogen ions, the plants grown under sodium light were chlorotic whereas the plants grown under fluorescent light remained green. The plants grown under sodium light released much less reductant from their roots and the roots reduced less Fe3+ to Fe2+ than did fluorescent-grown plants.

Conclusions Iron is essential in the biological world, and the manner in which the iron supply is made available to the plant is unique. Iron in the root environment of calcareous soils occurs most frequently in an oxidized state unavailable for plant use without the presence of modifying factors. Plants are classified as iron-efficient if they respond to iron-deficiency stress by inducing plant reactions that make iron available in a useful form, and they are classified as iron-inefficient if they do not. By comparing responses of iron-efficient and iron-inefficient plants to iron-deficiency stress, factors believed to enhance iron uptake have been documented. These factors are:

* release of iron-chelating compounds from roots,

* release of hydrogen ions from roots,

* release of reductants from roots, * reduction of Fe3" to Fe2+ by roots,

and * increases in organic acids (particu-

larly citrate) in roots.

No individual factor appears adequate to supply sufficient iron to the plant. However, both solubilization of iron and reduction of Fe3? to Fe2+ appear necessary, but solubilization of iron is not always accomplished in the same way. For example, the release of hydrogen ions may decrease the pH of the rhizosphere and solubilize iron, whereas the release of a phytosiderophore may also solubilize the iron without a decrease in pH. In both cases, reduction of ferric to ferrous iron by the root appears necessary for absorption/translocation of iron by the plant. The iron-inefficient plants that do not respond to iron- deficiency stress in the above manner die from a lack of iron.

Iron efficiency is genetically controlled, so biologists are challenged to select for iron efficiency in plants to be grown on calcareous soils. Iron- inefficient plants are good indicator plants for showing where iron is not available for proper plant growth. Efficient and inefficient plant genotypes exist for other essential micronutrients, such as boron, copper, manganese, molybdenum, and zinc. The mechanisms employed by these genotypes are yet to be determined.

4V. D. Jolley, J. C. Brown, and P. E. Nugent. 1988. Unpublished data.

References cited Ambler, J. E., J. C. Brown, and H. G. Gaugh.

1971. Sites of iron reduction in soybean plants. Agron. J. 53: 95-97.

Barrett-Leonard, E. G., H. Marschner, and V. Romheld. 1983. Mechanism of short term Fe(III) reduction by roots. Evidence against the role of secreted reductants. Plant Physiol. 73: 893-898.

Bell, W. D., L. Bogorad, and W. J. McIlrath. 1958. Response of the yellow-stripe maize mutant (ysl) to ferrous and ferric iron. Bot. Gaz. 120: 36-39.

Bienfait, H. F., J. Duivenvoorden, and W. Verkerke. 1982. Ferric reduction by roots of chlorotic bean plants: indication for an en- zymatic process. J. Plant Nutr. 5: 451-456.

Bjorkman, 0., and J. Berry. 1973. High efficiency photosynthesis. Sci. Am. 288: 80-93.

Brown, J. C. 1961. Iron chlorosis in plants. Adv. Agron. 13: 329-369.

.1978. Mechanism of iron uptake by plants. Plant Cell Environ. 1: 249-257.

Brown, J. C., and J. E. Ambler. 1974. Iron stress response in tomato (Lycopersicon esculentum). 1. Sites of fereduction, absorption




and transport. Physiol. Plant. 31: 221-224. Brown, J. C., and R. L. Chaney. 1971. Effect of

iron on the transport of citrate into the xylem of soybean and tomatoes. Plant Phys- iol. 47: 836-840.

Brown, J. C., R. L. Chaney, and J. E. Ambler. 1971. A new tomato mutant inefficient in the transport of iron. Physiol. Plant. 25: 48-53.

Brown, J. C., C. D. Foy, J. H. Bennett, and M. N. Christiansen. 1979. Two light sources (LPS and CWF) differentially affected Fe3+ reduction and growth of cotton. Plant Phys- iol. 63: 692-695.

Brown, J. C., R. S. Holmes, and L. O. Tiffin. 1958. Iron chlorosis in soybeans as related to genotype of rootstock. Soil Sci. 86: 75-82.

. 1961. Iron chlorosis in soybeans as related to the genotype of rootstock. 3. Chlo- rosis susceptibility and reductive capacity at the root. Soil Sci. 91: 127-132.

Brown, J. C., and L. O. Tiffin. 1965. Iron stress as related to the iron and citrate occurring in stem exudate. Plant Physiol. 40: 395-400.

Byers, B. P. 1986. Siderophores and biological systems. An overview. Pages 1-6 in T. R. Swinburne, ed. Iron, Siderophores and Plant Diseases. NATO ASI Series. Plenum Press, New York.

Camp, S. D., V. D. Jolley, and J. C. Brown. 1987. Comparative evaluation of factors in- volved in Fe stress response in tomato and soybean. J. Plant Nutr. 10: 423-442.

Chaney, R. L., J. C. Brown, and L. O. Tiffin. 1972. Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol. 50: 208-213.

Clark, R. B., and J. C. Brown. 1974. Internal root control of iron uptake and utilization in maize genotypes. Plant Soil 40: 669-677.

Frahn, J. L. 1958. The photochemical decom- position of the citrate-ferric-iron complex. A study of reaction products by paper iono- phoresis. Aust. J. Chem. 11: 399-405.

Jolley, V. D., and J. C. Brown. 1985. Iron stress response in tomato affected by potassium and renewing nutrient solution. J. Plant Nutr. 8: 527-541.

. In press. Iron efficient and inefficient oats. I. Differences in phytosiderophore release. J. Plant Nutr.

Jolley, V. D., J. C. Brown, M. J. Blaylock, and S. D. Camp. 1988. A role for potassium in the use of iron by plants. J. Plant Nutr. 11: 77-91.

Jolley, V. D., J. C. Brown, J. Pushnik, and G.

Miller. 1987. Effects of ultra-violet (UV)- blue light radiation on the growth of cotton. I. Effect on iron nutrition and iron-stress response. J. Plant Nutr. 10: 333-351.

Kramer, D., V. Romheld, E. Landsberg, and H. Marschner. 1980. Induction of transfer-cell formation by iron deficiency in the root epidermis of Helianthus annuus. Planta 147: 335-339.

Krauskopf, K. B. 1972. Geochemistry of micronutrients. Pages 7-40 in J. J. Mortvedt, P. M. Giordano, and W. L. Lindsay, eds. Micron- utrients in Agriculture. Soil Science Society of America, Madison, WI.

Landsberg, E. C. 1982. Transfer cell formation in the epidermis: a prerequisite for Fe- efficiency? J. Plant Nutr. 5: 415-432.

. 1984. Regulation of iron-stress- response by whole plant activity. J. Plant Nutr. 7: 609-621.

Latimer, W. M. 1952. Oxidation Potentials. Prentice Hall, New York.

Lindsay, W. L., and A. P. Schwab. 1982. The chemistry of iron in soils and its availability to plants. J. Plant Nutr. 5: 821-840.

Marschner, H., A. Kalisch, and V. Romheld. 1974. Mechanism of iron uptake in different plant species. Pages 273-281 in J. Wehrman, ed. Plant Analysis and Fertilizer Problems. vol. 2. German Society of Plant Nutrition, Hanover, FRG.

Marschner, H., V. Romheld, and M. Kissel. 1986. Different strategies in higher plants in mobilization and uptake of iron. J. Plant Nutr. 9: 695-713.

1987. Localization of phytosiderophore release and of iron uptake along intact barley roots. Physiol. Plant. 71: 157-162.

McDaniel, M. E., and D. J. Dunphy. 1978. Differential iron chlorosis of oat cultivars. Crop Sci. 18: 136-138.

Mino, Y., T. Ishida, N. Ota, M. Inoue, K. Nomoto, T. Takemoto, H. Tanaka, and Y. Suguira. 1983. Mugineic acid-iron(III) complex and its structurally analogous cobalt(III) complex: characterization and implication for absorption and transport of iron in graminaceous plants. J. Amer. Chem. Soc. 105: 4671-4676.

Neilands, J. B. 1981. Microbial iron compounds. Ann. Rev. Biochem. 50: 715-731.

Olsen, R. A., J. H. Bennett, D. Blume, and J. C. Brown. 1981. Chemical aspects of the Fe stress response mechanism in tomatoes. J. Plant Nutr. 3: 905-921.

Olsen, R. A., and J. C. Brown. 1981. Light- induced reduction of Fe3+ as related to causes of chlorosis in cotton. J. Plant. Nutr. 3: 767-787.

Pushnik, J. C., G. W. Miller, V. D. Jolley, J. C. Brown, T. D. Davis, and A. M. Barnes. 1987. Influences of ultra-violet (UV)-blue light radiation on the growth of cotton. II. Photo- synthesis, leaf anatomy, and iron reduction. J. Plant Nutr. 10: 2283-2297.

Romheld, V., and H. Marschner. 1986. Evi- dence for a specific uptake system for iron phytosiderophore in roots of grasses. Plant Physiol. 80: 175-180.

Schroder, K. H. 1964a. Complex formation with trivalent iron and N'ethylenebis[2(0- hydroxyphenyl)]glycine. Nature 202: 898- 899.

. 1964b. A study of the polarographic behavior of Niethylenebis[2(0-hydroxyphenyl)]glycine in the presence of iron ions. Acta Chem. Scand. 18: 596-602.

Sijmons, P. C., and H. F. Bienfait. 1984. Mech- anism of iron reduction by roots of Phaseo- lus vulgaris. J. Plant Nutr. 7: 687-693.

Takagi, S. 1976. Naturally occurring iron- chelating compounds in oat- and rice- washings. I. Activity measurement and pre- liminary characterization. Soil Sci. Plant Nutr. 22: 423-433.

Takagi, S., K. Nomoto, and T. Takemoto. 1984. Physiological aspects of mugineic acid, a possible phytosiderophore of graminaceous plants. J. Plant Nutr. 7: 469-477.

Tiffin, L. 0. 1966. Iron translocation. I. Plant culture, exudate sampling, iron-citrate analysis. Plant Physiol. 41: 510-514.

. 1972. Translocation of micronutrients in plants. Pages 199-229 in J. J. Mortvedt, P. M. Giordano, and W. L. Lindsay, eds. Mi- cronutrients in Agriculture. Soil Science So- ciety of America, Madison, WI.

Tiffin, L. 0., and J. C. Brown. 1961. Selective absorption of iron from iron chelates by soybean plants. Plant Physiol. 36: 710-714.

Tiffin, L. O., J. C. Brown, and R. W. Krauss. 1960. Differential absorption of metal chelate components by plant roots. Plant Phys- iol. 35: 362-367.

Wann, E. V., and W. A. Hills. 1973. The genetics of boron and iron transport in the tomato. J. Hered. 64: 370-371.

Weiss, M. G. 1943. Inheritance and physiology of efficiency in iron utilization in soybeans. Genetics 28: 253-268.

September 1989 551



Documents

Plant Metabolic Responses to Iron-Deficiency Stress