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Cuticular retention, foliarabsorption and translocationof Fe, Mn and Zn supplied inorganic and inorganic formMireille Ferrandon a & André R. Chamel aa Laboratoire de Biologie Végétale, DRF/LBIO,CENTRE D'ETUDES NUCLEAIRES DE GRENOBLE,85 X, GRENOBLE CEDEX, F‐38041, FrancePublished online: 21 Nov 2008.

To cite this article: Mireille Ferrandon & André R. Chamel (1988) Cuticularretention, foliar absorption and translocation of Fe, Mn and Zn supplied inorganic and inorganic form, Journal of Plant Nutrition, 11:3, 247-263, DOI:10.1080/01904168809363800

To link to this article: http://dx.doi.org/10.1080/01904168809363800

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JOURNAL OF PLANT NUTRITION, 11(3), 247-263 (1988)

CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION

OF Fe, Mn AND Zn SUPPLIED IN ORGANIC

AND INORGANIC FORM

Keywords : Cuticular retention, foliar absorption, translocation,

iron, manganese, zinc, EDTA-Fe, EDTA-Zn, EDTA-Mn.

Mireille FERRANDON and André R. CHAMEL

Laboratoire de Biologie Végétale, DRF/LBIO,

CENTRE D'ETUDES NUCLEAIRES DE GRENOBLE, 85 X,

F-38041 GRENOBLE CEDEX, France.

ABSTRACT

As chelates are commonly used in practice for soil

fertilization and the interest of their extension to foliar

fertilization is still in discussion, the purpose of this study

was to specify some aspects of their behaviour when applied to

leaves in comparison with inorganic forms. Since the first barrier

to overcome in foliar nutrition is the cuticle, experiments were

carried out with isolated Tomato fruit cuticles considered as

model, in order to compare the cuticular affinities for

respectively, inorganic and organic (EDTA) forms of iron,

manganese and zinc. It was found that, except in the case of iron

where no significant difference was observed, the cuticular

Sorption was lower with EDTA than with the inorganic forms.

247

Copyright © 1988 by Marcel Dekker, Inc.

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248 FERRANDON AND CHAMEL

Parallel experiments were performed on whole Pea plants, in order

to measure the levels of absorption and translocation in situ of

Fe, Mn and Zn applied on leaves, in the form of either the EDTA

chelate or the sulfate salt. For both kinds of compounds extensive

fixation occurred in the treated area. The three elements were

less absorbed as chelates than as inorganic salts, in accordance

with results on isolated cuticles, while further translocation

within the plant was much greater with chelates. However, the

combination of these two parameters, uptake and translocation,

sometimes raises the question of the actual interest of chelates

as foliar fertilizers with respect to their higher cost, and that

without regard to any possible positive effect they may have on

other components of the yield.

INTRODUCTION

When micronutrients are provided as foliar sprays on crops,

for example in order to prevent specific deficiencies at critical

stages of plant growth, the entry of the trace-element depends

on many factors, such as characteristics of the leaves and

particularly of their cuticles, technical spraying features and

climatic conditions, and the chemical characteristics of the

applied solutions (1). Among the latter, the nature of the ligand

associated with the considered metal cation may be of great

significance for the ability of the compound to move across the

cuticle and the underlying tissues before uptake by vascular

bundles.

If many soil-experiments were carried out in order to compare

the relative efficiency of organic and inorganic metal-carriers,

as those of Holmes and Brown 1955, Kroll 1957, Ellis et al. 1970,

Schneider, Chesnin and Jones 1968, cited by Murphy and Walsh 1972

(18), and others (9, 14, 15, 18, 23, 30, 32), the reports of such

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CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION 249

studies with respect to foliar fertilization are limited (5, 17,

21, 31, 33). Our purpose was firstly to determine the cuticular

affinity for the three micronutrients in relation to their

chemical ligand by means of the determination of their retention

by isolated Tomato fruit cuticles. This might give a better

understanding of their behaviour at the very start of

micronutrient uptake.

Secondly, absorption and translocation of the three elements

Fe, Mn and Zn were measured after their application in sulfate

or chelated form on young Pea plants. This was to check whether

the promoting effect of chelation on translocation, already

reported by several authors for Fe at least (6, 8, 34), was also

observed with Zn and Mn. This would then determine whether the

thus-derived advantage of an organic carrier is of sufficient

significance in the final decision concerning fertilization

policy.

MATERIALS AND METHODS

. Sorption measurements. These were carried out with cuticles

isolated from ripe Tomato fruits (Lyaopersiawn esaulentim), which

proved to be a useful material as regards easy and quickly

achieved enzymic isolation (2) ; it will be assumed that the

results obtained with these cuticles can also be carried over to

cuticles from other organs and species, such as the leaves of Pea

plants for instance, since cuticles have been found to be ionic

exchangers with isoelectric point around 3 (22) and thus may

present some common physico-chemical properties.

Batches of ten cuticular discs (1 cm diameter) were immersed

with constant stirring in 5 ml of a solution of the chosen trace-

element (0.1 raM-initial pH of 6) containing the radioactive

isotope - 59p6j 54}^ o r 65zn - with a specific activity of 111

MBq/mmole. One batch was used at a time and per treatment.

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250 FERRANDON AND CHAMEL

At selected time intervals, the corresponding cuticles were

removed from the radioactive solution and, after excess solution

had been blotted off with filter paper, they were transferred to

10 ml of deionized water with three changes for 5 mn each. After

the last wash and once the cuticular discs had been air-dried,

they were submitted to radioactive assay with a gamma-counter (CG

4000 Intertechnique). The radioactive solution and the washing

liquids were also assayed by means of two samples of 1 ml each

in order to give an appraisement of the amounts of the elements

still in solution or removed through washing procedures.

Furthermore, samples from control vials containing the radioactive

solution without any cuticle were assayed so as to assess the

losses due to adsorption on the glass surface.

. Experiments with whole plants : These were carried out with

dwarf Pea plants (Pisum sativvm cv Douce Provence) since the

growth cycle was sufficiently short (fructification was achieved

within about 5 weeks) under growth chamber conditions (day : 12

h - 26°C - RH 60 %/night : 18°C - 80 % RH).

When the plants were about fifteen days old, the radioactive

solution was applied on one leaf per plant, about midway up the

stem, by means of a droplet of 10 pi deposited on an area

previously wetted with Tween 20 1 "L. This area was in the middle

of the blade, that is, near the midrib. The characteristics of

the radioactive solution were the same as for sorption experiments

except for the specific activity, which was much higher (740 MBq/

mmole) due to the low translocation from the treated area.

The droplets were allowed to dry in the laboratory and the

plants were then settled back in the growth chamber. At the end

of the 24 h experiment, the treated leaf was sectioned and washed

twice in 15 ml of deionized water for 5 mn. The treated area was

removed with a corkborer and the other plant parts were separated

as follows :

- leaves and stem above the treated leaf (H) ;

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CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION 251

- leaves and stem below the treated leaf (B), including the

opposite leaf ;

- roots (R).

Each part was assayed for radioactivity directly on fresh

material.

RESULTS

Cuticular retention of Fe, Mn and Zn : The cuticular

retention was expressed either directly in terms of nanomoles per

cuticular disc or by the concentration ratio :

nanomoles/g of cuticle

nanomoles/mi of the radioactive solution at the end of the experiment

Figure 1 reveals some variation of the cuticular retention

in relation to the chemical form but results depend on the element

considered : for both elements Zn and Mn the cuticular Sorption

was significantly higher with the inorganic form (sulfate and

chloride) in comparison with the organic one, and there was no

significant difference between the two inorganic salts. In the

case of iron, no significant difference was found between the

three sources of this element in spite of slightly higher values

with EDTA.

These observations are confirmed by data presented in table

1. Some evidence is indicated of high sorption by plant cuticles

of the three elements studied as the concentration of these

elements in the cuticles is much higher than in the solution.

Despite their lower sorption on isolated cuticles, the EDTA

chelates of Fe, Mn and Zn do not seem more susceptible to washing

than the inorganic salts (table 2). Indeed, in the case of Mn or

Fe, for example, they are less so.

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252 FERRANDON AND CHAMEL

Table 1 : Ratios of the final Concentration of Iron, Manganeseand Zinc respectively, between the Cuticle and the RadioactiveSolution as a function of Time and Chemical Form (Sulfate,Chloride or EDTA Complex - 0.1 mM - 111 MBq/mtnole ). Datacorrespond to different batches : one/time/treatment. Statisticswere obtained with pairwise t~tests.

TIME FeSC-4 Fe EDTA FeCl3

30 mn

1 h

4 h

48 h

72 h

96 h

TIME

82

81

98

/

142

202

no significant

MnSC-4

71

90

139

316

340

252

difference

Mn EDTA

/

114

147

110

150

151

MnCl2

30 mn / / 679

1 h 1167 76.2 743

4 h 900 96.7 /

24 h 1288 / /

48 h 1592 92.5 1081

72 h 1167 53.1 772

significant difference between MnSC>4 and MnCl2MnSO^ and Mn EDTA

P = 0.05 MnCl2 and Mn EDTA

TIME

30 mn

1 h

4 h

24 h

48 h

72 h

ZnSO4

1046

1386

2382

3316

3880

4823

Zn EDTA

153

188

281

288

/

ni

ZnCl2

/

1231

2656

3718

3598

5642

(ZnSÛ4 - ZnCl2)/Zn EDTA ! significant difference : P = 0.05

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CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION 253

Table 2 : Amounts (nraoles) of either Mn, Zn or Fe found in WashingSolutions (3 changes) after Retention Experiments (72 h) with theThree Sources : sulfate-EDTA-chloride.

S04 - EDTA - C12/C13

Mn

Zn

Fe

1st

2nd

3rd

1st

2nd

3rd

1st

2nd

3st

36.0 ± 4.4

41.0 ± 1.8

43.0 ± 0.2

4.0 ± 0.0

1.0 ± 0.2

1.0 ± 0.2

57.0 ± 4.6

24.0 ± 0.6

17.0 + 0.7

0

0

6.0 ± 0.7

5.0 ± 0.1

4.0 ± 0.0

2.0 ± 0.3

12.0 ± 1.0

2.0 + 0.0

3.0 + 0.1

56.0 + 2.2

37.0 ± 3.0

28.0 + 1.0

7.0 + 0.1

0

0

76.0 ± 2.0

26.0 ± 1.5

13.0 ± 0.3

Absorption and translocation of Fe, Mn and Zn following foliar

applications.

It clearly appears with the three elements that foliar uptake

is better with the inorganic form than with the organic form

(fig. 2), which is consistent with other findings (13). However,

the proportion remaining in the treated area (T.A.) is less

important, though still very high, when the micronutrient is

applied as the EDTA complex. The percentage translocated from the

treated leaf (= T.A. + L) is also higher with the organic form

than with the sulfate.

These results are summarized in table 3, with washing data ;

with EDTA complex high losses are indicated at the first wash,

which is in accordance with the low absorption previously observed

on figure 2.

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254 FERRANDON AND CHAMEL

10. nanomoles Fe / cuticular disc

nanomoles Mn / cuticular dis

MnS04 MnEDTA HnC12

nanomoles Zn / cuticular disc

* I30-1

ZnS04 ZnEDTA ZnC12

Fig, 1 : Cuticular Sorption (nanomoles/cuticular disc) of iron, mangane

and zinc as a function of time and chemical form (mean ± Op)

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part of the plant

H

TA

L

8

R

part of the plant

H

X absorption

part of the plant

H

TA

L

X absorption

100

X Fe In the plant

100

% Mn In the plant

Fe - EDTA Mn-EDTA

part of the plant

H

TA

X absorption

100

X Fe In the plant

part of the plant

H

TA

L

100

X Mn In the plant

MnSCM

X absorption

100

X Zn In the plant

Zn-EDTA

part of the plant

H

TA

L

B

R

(

I

—u33

X absorption

50

H

100

X Zn In the plant

ZnSO4

FIG. 2 : Absorption (pie-diagram) and translocation (bar-diagram)of iron, manganese and zinc applied as sulfate or EDTAto one leaf of 15 day-old plants (Pisum sativum)

H: leaves and stem above the treated leafB: underR: rootsT.A.: treated area - L: lamina of the treated leaf minus

the treated area

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256 FERRANDON AND CHAMEL

Table 3 : Wash-out, Absorption and Translocation of Iron,Manganese and Zinc as Percentages of the Total Activity Recovered(10 replications-mean ± op) after Foliar Application in eitherEDTA of SO4 (1 mM-pH6740 MBq/mmole) form. Values in bracketsrepresent the sum of the organs H + B + R (see legend fig. 2)compared to the amount in the whole plant.

Fe EDTA Fe SO4

1st wash

2nd wash

54.5 ± 4.9

1.2 + 0.7

5.9 ± 4.9

2.5 ± 2.2

Total

Uptake

Translocationfrom the treated leaf

55.8 ± 5

44.2 ± 8

0.93 (2.

.6

.2

1)

8.4

91.5

0.18

± 7

± 8

(0.

.1

.2

2)

Mn EDTA Mn SO4

1st wash

2nd wash

86.5 ± 3.7

0.6 ± 0.9

0.4 ± 0.1

0.3 ± 0.1

Total

Uptake

Translocation

1st wash

2nd wash

Total

Uptake

Translocation

87.1

12.8

1.52

± 4.0

± 6.4

(11.9)

Zn EDTA

48.4

0.1

48.7

51.2

4.9

± 5.4± 0.0

± 9.4

± 13.3

(9.6)

0.8 ± 0.5

99.2 ± 13.9

0.19 (0.2)

Zn SO4

23.5 ± 6.21.9 ± 0.8

25.4 ± 10.6

74.5 ± 14.0

4.7 (6.3)

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CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION 257

DISCUSSION

The lower cuticular sorption of the micronutrients Zn and

Mn when supplied as chelates in retention experiments could be

attributed to the limited number of metal cations available for

retention by the negative sites of the cuticle ; the size of the

complex might also decrease the rate of binding on the surface

and access to inner sites. This latter explanation assumes that

the metal cation remains bound to its ligand during the cuticular

sorption and penetration. This assumption may be of significance

for explaining the different behaviour of iron compared to Zn and

Mn : although the sorption experiments were carried out with an

initial pH of 6, the pH value control at the end of each

experiment revealed that it reached neutrality. It can be assumed

that the inorganic compounds of the metal cations gave rise to

the ionic species Fe3+, Zn 2 + and Mn 2 +, and possibly to their

hydroxydes, especially in the case of iron. This would account

for the almost similar retention levels with the sulfate and

chloride compounds - in spite of the case of Mn - as far as the

only "free" ions are concerned. It would not be the case with the

EDTA complexes of Zn and Mn, still predominant, at pH 7, on the

corresponding "free" cations, while for iron this chelate would

no longer exist in solution due to ist lower stability with

increasing pH, especially at these very low concentrations where

extensive dilution occurs. In this respect, reference can be made

to Norvel's report on chemical species existing in soil solution,

despite the fact that this study included competing cations (20).

Thus, it would be interesting to investigate, especially with

iron, at a lower pH which might ensure the actual existence of

every tested chemical form in solution, that is : "free" ions with

inorganic salts and the complexed cations with organic compounds.

This would require the use of buffers in order to avoid pH

variations during the experiment, despite the risk of disturbing

equilibria between the chemical species in solution through

possible strong affinity of the buffer for the metal cation. In

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258 FERRANDON AND CHAMEL

this respect Good's buffer would preferentially be employed (10)

despite remarks made by other investigators (19).

The low sensitiveness of chelated compounds to washing

procedures in experiments with isolated cuticles is not in

disagreement with low cuticle sorption data in as much as the

strength of the retention on cuticular sites would not be

concerned but only the number of available binding sites. In

experiments with whole plants, the higher leakage of the EDTA

chelates through washes would account for compounds in excess on

the leaf and not bound to the cuticle.

As a matter of fact, it can be noted here that the notion

of uptake in experiments in situ may include an eventually high

proportion of compounds still retained within the cuticle, as

demonstrated in the investigation on isolated cuticles, and thus

not really absorbed by leaf tissues. This problem is all the more

acute as the washing procedures are carried out with deionized

water and the question is raised of the most suitable solution

to avoid misjudgements. This aspect has been fully developped in

a review by Smith and Storey (24) who compared several washing

techniques.

The high concentrations of the three elements studied

remaining in the treated area after 24 h may be related to their

low diffusion (7) and high retention in the cuticle, which would

have to be confirmed in situ with more acute investigations, and

also to their low mobility within the plant (4, 12, 25, 26).

The lower uptake of the micronutrients provided in the form

of EDTA in situ can be connected with their lower cuticular

sorption. However, their higher mobility has already been reported

in the literature (3, 11, 16), which suggests that the ion is not

separated from its organic carrier, neither during the penetration

process nor within the plant, despite some contradictory

assumptions emitted by Tiffin (28) or Wittwer and Bukovac (34).

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CUTICULAR RETENTION, FOLIAR ABSORPTION AND TRANSLOCATION 259

The organic ligand might play the role of a carrier ensuring

translocation of the cations in place of a natural carrier

occurring in the plant, e.g. citrate for Iron (25, 29).

Despite the difficulties of extrapolating laboratory

experiments to field conditions - particularly if we consider the

great difference in view of growing and climatic conditions or

application techniques, we can already try to evaluate the actual

interest of the use of organic chelates as foliar fertilizers by

expressing our results in terms of efficiency.

If only the uptake parameter is taken into account, for

example when deficiency symptoms are to be corrected in a short

time and locally on the plant the EDTA complexes of Iron,

Manganese and Zinc are respectively (°¿ in the plant/initial

supply =) 2, 7.7 and 1.4 times less effective than the sulfate

salt (provided that the experiments lasted no longer than 24 h

and that the fraction still in the treated area remains at least

partly available for the plant as a kind of reservoir).

However, if translocation is the only considered factor, with

the purpose of supplying micronutrients to the whole plant after

a certain time and particularly to new growing organs, chelates

appear to be (% translocated from the treated leaf/% in the

plant =) 10, 60 and 1.5 more efficient than the inorganic salts

of Fe, Mn and Zn after 24 h.

Combining both these parameters, that is by expressing

results of translocation in terms of percentages of the initial

supply translocated after 24 h from the treated leaf, our data

give the efficiency rates of about 5, 8 and 1 for the chelates

of Fe, Mn and Zn compared with the sulfate sources.

Considering the high cost of organic chelates as opposed to

classic fertilizers such as sulfate salts, the advantage of the

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260 FERRANDON AND CHAMEL

former over the latter must be sufficient to justify their use.

This seems to be the case of Fe and Mn here, but not of Zn.

However, it must be noted that our experiments were performed with

plants growing under sufficient nutrition conditions which is not

the usual case for field experiments when specific treatments are

required. Indeed, these are performed under conditions of nutrient

deficiency. The respective efficiency of chelates and inorganic

salts may be greatly modified by deficiency conditions and further

study is required.

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2. CHAMEL, A. et B. BOUGIE. 1977. Absorption foliaire du cuivre :étude de la fixation et de la pénétration cuticulaires.Physiol. Vég. 15 : 679-693.

3. CHEBOTINA, M.Y. 1972. Penetration of 65Zn into plants throughthe leaves. Sov. J. Ecol. 3 : 469-470.

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