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Iron chlorosis paradox infruit treesFermín Morales a , Roberto Grasa a ,Anunciación Abadía a & Javier Abadía aa Departamento de Nutrición Vegetal ,Estación Experimental de Aula Dei, ConsejoSuperior de Investigaciones Científicas , Apdo.202, Zaragoza, E‐50080, SpainPublished online: 21 Nov 2008.

To cite this article: Fermín Morales , Roberto Grasa , Anunciación Abadía &Javier Abadía (1998) Iron chlorosis paradox in fruit trees, Journal of PlantNutrition, 21:4, 815-825, DOI: 10.1080/01904169809365444

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JOURNAL OF PLANT NUTRITION, 21(4), 815-825 (1998)

Iron Chlorosis Paradox in Fruit Trees

Fermín Morales, Roberto Grasa, Anunciación Abadía, andJavier Abadía

Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei,Consejo Superior de Investigaciones Científicas, Apdo. 202, E-50080Zaragoza, Spain

ABSTRACT

We have investigated the effect of iron (Fe) chlorosis on leaf Fe, leaf chlorophyll,leaf area, leaf thickness, leaf fresh and dry weight and specific leaf weight perarea in young, fully developed leaves of Fe-deficient and Fe-sufficient peach(Prunus persica L. Batsch) and pear (Pyrus communis L.) trees growing in thefield in northeastern Spain. Iron chlorosis decreased leaf chlorophyllconcentration, fresh and dry weight per leaf and leaf area, whereas leaf thicknesswas practically unaffected. Chlorosis caused differences in leaf Feconcentrations that were best detected on a per leaf basis. Significantdifferences in Fe concentration could be detectable in pear on an area basis ora volume basis. However, when expressed on a per dry weight basis the Feconcentrations of control and chlorotic leaves were not significantly different.The fact that chlorotic leaves have less Fe per leaf confirms that the chlorotictrees are under a short supply of Fe. However, chlorotic fruit tree leaves havemuch higher leaf tissue Fe concentrations than Fe-deficient plants grownunder controlled conditions, which suggests that Fe may be immobilizedsomewhere in the chlorotic leaf in an unavailable form.

815

Copyright © 1998 by Marcel Dekker, Inc.

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816 MORALES ET AL.

INTRODUCTION

One of the analytical techniques used to study Fe deficiency (Fe chlorosis) isthe measurement of the total Fe concentration in leaves. However, this approachpresents major problems because the data obtained from plants grown in controlledenvironments are different from those obtained with field-grown plants (Terry andAbadía, 1986; Abadía, 1992). It has been established that when plants grow underFe deficiency in controlled environments, the total leaf Fe concentration (on a drymatter or an area basis) is generally low compared to Fe-sufficient plants (Terry,1980; Terry and Low, 1982;Koleschetal., 1984). Under these conditions, linearrelationships are usually found between the Fe and leaf chlorophyll concentrations(Terry, 1980).

However, when leaves from Fe-deficient plants grown in the field are analyzed,the leaf Fe concentrations have been found to be relatively high in many cases(Oserkowsky, 1933;Fallade, 1972;Pateletal., 1977;Kovancietal., 1978; van denDriessche, 1978; Mengeletal., 1979; Carter, 1980; Venkatraju and Marschner, 1981;Chen and Barak, 1982; Hamze and Nimah, 1982; Mengel and Malissiovas, 1982;Mengel and Biibl, 1983; Mengel et al., 1984; Abadía et al., 1985; Mengel andGeurtzen, 1988;Abadíaetal., 1989). Furthermore, under field conditions the totalleaf Fe concentration is not well correlated with the leaf chlorophyll concentration(Hamze and Nimah, 1982; Procopiou and Wallace, 1982; Mengel et al., 1984;Häusslingetal., 1985).

The fact that Fe-chlorotic leaves often have high Fe concentrations has beenrecently termed the (Fe) "chlorosis paradox" (Römheld, 1997). This apparent paradoxhas been traced to the effect of Fe chlorosis on leaf growth. Reductions in leafgrowth would produce apparently high Fe concentrations on a dry matter basis,even when the Fe per leaf is reduced by Fe chlorosis (Römheld, 1997).

The aim of this work was to provide additional information on the Fe "chlorosisparadox" that is known to occur in leaves of peach (Abadía et al., 1985) and peartrees (Abadía et al., 1989) growing in the Ebro valley area in northeastern Spain;this is one of the mediterranean agricultural areas where Fe chlorosis is a majorproblem (Sanz et al., 1992). The relatively large amounts of leaf Fe found in chloroticpeach and pear leaves suggest that Fe may be immobilized in an unavailable formsomewhere in the leaf.

MATERIALS AND METHODS

Plant Material

Leaves were collected from peach {Prunus pérsica L. Batsch) and pear (Pyruscommunis L.) trees growing in calcareous soils and affected by iron chlorosis.Orchards were located in two sites named 'El Temple' (El Temple, Huesca, Spain)and 'San Bruno', in the Servicio de Investigación Agroalimentaria-DiputaciónGeneral de Aragón farm, located in the Aula Dei Campus (Zaragoza, Spain). The

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IRON CHLOROSIS PARADOX IN FRUIT TREES 817

former has commercial orchards with good fertilization and the latter is in anexperimental orchard with poor nutrition. The soil of'El Temple' site has a clay-loamy texture, with 32% total calcium carbonate, 12.6% active lime, 1.89% organicmatter, pH in water 8.4. The soil of the 'San Bruno' site has a clay-loamy texture,with 31% total calcium carbonate, 9.9% active lime, 2.86% organic matter, pH inwater 8.0. At the 'San Bruno' site a pear orchard, cultivar 'Blanquilla' ('Agua deAranjuez') grafted on quince A EM, with a frame 5x4 m, 20 years old, was used. Atthe 'El Temple' site we studied a pear orchard, cultivar 'Blanquilla' grafted onquince B A29,17 years old, trained as palmette, with a frame of 3x4 m, and a peachorchard, cultivar 'Babygold T grafted on seedling, 17 years old, with a frame of 4x5m. The orchards had not been treated with Fe chelates in the last two or threeyears. Under these conditions chlorosis became more marked in the orchardsstudied every year. In all three orchards in the 1997 growing season there weretrees with marked chlorosis symptoms and other trees that still remained green.Leaf samples were taken from both tree categories.

Fully developed leaves were taken from the distal third of the current year'sgrowth (3rd-6th and 5th-8th leaves from top in pear and peach, respectively) by theend of June, 1997. Samples were transported from the orchards to the laboratory asquickly as possible for processing. Samples from each orchard were divided intothree or four categories of chlorosis (measured with the SPAD meter). Leaf thicknesswas determined in each leaf with a portable analogic thickness meter (Ascaso,Huesca, Spain). Each leaf was separated in leaf blade, petiole and main veinsections. The fresh (FW) and dry weight (DW) of each leaf blade was determined.Specific leaf weight per area (SLW) was estimated by drying and weighing a knownsurface of leaf blade tissue (ten leaf disks, 9.5 cm2 total area). The area of the leaveswas estimated by weighing xerox copies of each leaf, calibrated with xerox copiesof a known surface. Other measurements using a) the DW and SLW values and b)leaf area meters gave similar values (data not shown).

Chlorophyll Analysis

The chlorophyll concentration per area was estimated in the field by using aSPAD meter (Minolta). For calibration leaf disks were first measured with theSPAD, then frozen in liquid N2, extracted with 100% acetone in the presence of Naascorbate (Abadía and Abadía, 1993) and the extracts analyzed spectro-photometrically according to Lichtenthaler ( 1987).

Measurements of Leaf Iron

The leaf blade tissue from groups of 4-5 leaves each (4 replications per chlorophylllevel in each of the orchards) was washed with standard procedures (Abadía et al.,1989), oven-dried at 60°C and analyzed for Fe by atomic absorptionspectrophotometry as indicated previously (Abadía et al., 1985). For the calculationsof the Fe concentration on basis other than DW, the DW, SLW and thickness datacorresponding to the same leaves analyzed for Fe were used.

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818 MORALES ET AL.

RESULTS

Effect of Chlorosis on Leaf Chlorophyll

Iron chlorosis decreased markedly the leaf chlorophyll concentration in all threeorchards (Table 1). In the peach orchard chlorophyll decreased by 60%, whereasin pear the decrease was between 94 and 91 %. These decreases are typical examplesof the strong reduction in chlorophyll caused by Fe deficiency in the area studied.

Effect of Chlorosis on Leaf Morphological Characteristics

Leaf thickness was little affected by iron chlorosis. A small decrease in thickness(approximately 12%) was observed in one of the pear orchards ('San Bruno')(Table 1). In the other orchards the leaf thickness was unaffected.

Iron chlorosis induced significant decreases in the DW and FW per leaf. Thereduction in leaf DW caused by chlorosis in the peach orchard was 47%. In thetwo pear orchards ('El Temple' and 'San Bruno') leaves showed maximal DWreductions of 46% and 43%, respectively (Table 1). The FWper leaf was decreasedin chlorotic leaves by 36%, 29% and 29% in the peach orchard ('El Temple') and thetwo pear orchards ('El Temple' and 'San Bruno'), respectively, when compared tocontrol leaves (Table 1). The fact that the decreases in FW were not as marked asthe decreases in DW could be explained by the fact that leaves were sampled atmidday, when the water status was better in the chlorotic than in the control treesdue to early stomatal closure (data not shown).

The leaf size of peach and pear was also decreased in response to iron chlorosis.In peach the reduction in leaf area caused by chlorosis was 41%. In the two pearorchards ('El Temple' and 'San Bruno') leaves showed maximal reductions in areaof 30 and 12% of the control values, respectively (Table 1). In the pear orchard withpoor nutrition ('San Bruno') leaf size, leaf thickness and DW and FWper leaf weregenerally smaller than in the well fertilized one ('El Temple') (Table 1).

The SLW was also decreased by Fe chlorosis in peach and pear. The reductionin leaf SLW caused by chlorosis in the peach orchard was 10%. In the two pearorchards ('El Temple' and 'San Bruno') leaves showed SLW reductions of 23%and 35%, respectively (Table 1). Reductions in the SLW with chlorosis ofapproximately 33% were found in a previous work in a different pear orchard(Abadía et al., 1989).

Effect of Chlorosis on Leaf Iron Concentrations

Chlorotic leaves of both peach and pear had lower Fe concentrations expressedon a DW basis than control leaves, but the differences were not statistically different.Peach chlorotic leaves had 84-91 fig Fe g DF1, whereas control leaves hadapproximately 130 ug Fe g DF1 (Table 2). These differences were not significantlydifferent because the standard deviations were quite high. The concentrationsfound here compare to values of 63-80 and 76-100 ng Fe g DF1 found previously

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TABLE 1.treatment.

Leaf morphological parameters of control and chlorotic peach and pear leaves. Data are the mean ± SD of 17 to 29 leaves per

In

5Species and Location

|Fe status |

Peach, El Temple[+Fe][-Fe][-Fe]

Pear, El Temple[+Fe][-Fe][-Fe][-Fe]

Pear, San Bruno[+Fe][-Fe][-Fe][-Fe]

Chlorophyll

(nmol.cm'2)

27.4±5.9 a*17.5±5.6 b10.9+5.9 c

66.0+3.2 a16.3±3.3 b8.0±3.1 c4.2±3.1 d

46.6±3.0 a13.912.9 b7.2±2.9 c4.2±3.1 d

Leaf thickness(mm)

0.1810.01 a0.1810.01 a0.18+0.01 a

0.27+0.02 a0.2610.02 a0.2810.02 a0.2610.03 a

0.2510.03 a0.2210.01 b0.2310.01 b0.2210.01 b

DW.Ieaf1

(g)

0.30+0.03 a0.2410.02 b0.1710.02 c

0.26+0.02 a0.22+0.03 b0.2110.05 b0.14+0.03 c

0.21+0.02 a0.1710.01 b0.14+0.01 c0.12+0.02 d

FW.Ieaf1

(g)

0.9110.070.7710.050.58+0.06

0.6310.080.57+0.110.5410.130.4510.12

0.4210.030.3810.010.3410.010.30+0.04

abc

aaab

abcd

Area.leaf'(cm2)

45.113.0 a38.2+0.9 b27.913.0 c

28.615.0 a25.713.5 a22.9+3.6 b20.0+5.0 c

22.013.7 a21.513.1 a17.9+2.9 b19.313.0 b

SLW

(mg.cnT2)

6.6+0.2 a6.410.3 ab6.010.2 b

9.111.1 a8.611.2 a9.211.8 a7.011.6 b

9.611.3 a7.910.8 b7.810.9 b6.211.0 c

oX

3G

S

•Means followed by the same letter were not significantly different (Student's test) at the p<0.05 probability level.

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820 MORALES ET AL.

for chlorotic and control peach leaves in the same area (Abadía et al., 1985). Pearchlorotic leaves had 84-123 ('El Temple') and 137-139 ugFe g DP1 ('San Bruno')whereas control leaves had 150 and 167 ug Fe g DF~' in 'El Temple' and 'SanBruno,' respectively (Table 2). In a previous work we found 135-150 and 110-150Hg Fe g DF"1 in Fe-deficient and control pear leaves, respectively (Abadía et al.,1989).

When the Fe concentration in leaves was expressed on an area basis, chloroticleaves had generally less Fe than control leaves. Peach leaf Fe per area wasreduced by chlorosis from approximately 0.86 to 0.54-0.55 ug Fe cm2, although thedifference was only significant at the pO.10 level (Table 2). In pear, chlorosisdecreased significantly the Fe concentration per area. The most chlorotic pearleaves had 0.59 ('El Temple') and 0.87 ug Fe cm'2 ('San Bruno') whereas controlleaves had 1.37 and 1.60 Ug Fe cm'2, in 'El Temple' and 'San Bruno', respectively(Table 2). These values indicate that chlorosis decreased the Fe concentration perarea in pear by 46-57%. These data confirm the view that the area basis establishesdifferences between control and chlorotic leaves better than the dry matter basis(Heras et al., 1971 ). Similar results were obtained when the concentrations of Fewere expressed on a leaf volume basis (Table 2).

When the Fe concentration in leaves was expressed on a per leaf basis, chloroticleaves had significantly less Fe than control leaves. The most chlorotic peachleaves had 15 ug Fe leaf1, whereas control leaves had approximately 39 ug Fe leaf-1 (Table 2). Therefore, chlorosis decreased the Fe concentration per leaf by 63% inpeach. The most chlorotic pear leaves had 12 ('El Temple') and 17 ugFeleaf1 ('SanBruno') compared to 39 and 35 ug Fe leaf, in control leaves of'El Temple' and'San Bruno', respectively (Table 2). These data indicate reductions in the amountof Fe per leaf of 70% and 53% in pear grown at 'El Temple' and 'San Bruno',respectively.

DISCUSSION

Our data indicate that Fe chlorosis causes significant decreases in the area, FWand D W of the fully expanded leaves that are usually sampled for mineral analysis,both in peach and in pear. Chlorosis also induces decreases in the SLW.

The data indicate that Fe deficiency caused differences in leaf Fe concentrationsthat are best detected on a per leaf basis. Significant differences in Fe concentrationcould be detectable in pear on an area basis or a volume basis, although thesebases do not consider the decrease in leaf size caused by Fe deficiency. However,when expressed on a dry weight basis, the Fe concentrations of control and chloroticleaves were not significantly different. The reason for this is that not only the Feconcentration per area, but also the SLW values decrease with chlorosis.

The fact that chlorotic leaves have less Fe per leaf confirms that the chlorotictrees are under a short supply of Fe. This supports the view put forward byRömheld (1997) that the apparent high Fe concentrations on a DW basis are ratherthe consequence, and not the cause, for Fe chlorosis.

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TABLE 2. Leaf Fe concentrations in control and chlorotic peach and pear leaves, expressed on several baseis. Data arethe mean ± SD of 4 replications, each composed by 4-5 individual leaves.

Species and Location

|Fe statusl

Peach, El Temple[+Fe][-Fe][-Fe]

Pear, El Temple[+Fe][-Fe][-Fe][-Fe]

Pear, San Bruno[+Fe][-Fe][-Fe][-Fe]

Chlorophyll(nmol.cnT^)

27.417.510.9

66.016.38.04.2

46.613.97.24.2

LeafFe(ppm)Olg.gDW1)

I29.7±33.4 a*84.2±14.4 a90.6±20.3 a

150.2±38.6 a122.9±21.0 a86.3±19.3 a83.7±18.7 a

167.4±43.0 a138.2+23.6 a137.3±30.7 a139.3±31.3 a

LeafFe

(Hg.cnT2)

0.86±0.24 a0.54±0.1O a0.55±0.11 a

1.3710.23 a1.05±0.15 b0.79±0.15 c0.59±0.14 d

1.6010.28 a1.0910.14 b1.0710.16 b0.8710.15 c

LeafFe(Hg.cnT3)

47.1113.5 a29.916.2 a30.915.6 a

50.616.6 a40.414.5 b28.214.3 c22.513.6 d

64.018.2 a49.7+3.9 b46.614.4 b39.314.7 c

LeafFe

(Hg.leaf1)

39.2+12.9 a20.514.0 ab15.113.5 b

39.116.5 a27.014.1 b18.114.2 c11.712.6 d

35.216.2 a23.512.7 b19.212.8 c16.713.3 d

•Means followed by the same letter were not significantly different (Student's test) at the p<0.05 probability level

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822 MORALES ET AL.

However, the data presented here indicate that Fe-chlorotic fruit tree leaveshave higher leaf tissue Fe concentrations than Fe-deficient plants grown undercontrolled conditions. For instance, severely Fe-deficient sugar beet leaves (4nmol chlorophyll cm2) usually have approximately 22 ug Fe g DF'1 (Terry, 1980) or0.08 ug Fe cnr2 (Terry and Low, 1982). Control and Fe-deficient leaves of applegrown in nutrient solution had 60 and 44-47 ug Fe g DW1, respectively (Ji et al.,1985). In peach rootstocks grown in hydroponics, control and Fe-deficient leavesmay have 47-92 and 14-56 ugFe g DP1, respectively (Romera et al., 1991a, 1991b).Peach and pear Fe-chlorotic leaves with approximately the same Chi concentrationgrowing in field conditions had approximately 84-139 ug Fe g DF"1 (0.55-0.87 ug Fecm"2) (Table 2). Therefore, Fe concentrations in field-grown leaves are generallyhigher than those found in leaves from plants grown in controlled environments.

The relatively high Fe concentrations found in Fe-deficient fruit tree leavessuggest that Fe may be accumulated in an unavailable form somewhere in thechlorotic leaf (Marschner, 1986, 1991). This could be of crucial importance indesigning new ways of controlling Fe chlorosis in fruit tree crops, because theseFe pools are potentially capable of being re-mobilized. In some species greeningmay occur when diluted ascorbic or sulfuric acid is fed to the petiole or injectedinto the chlorotic leaves (Diez-Altares, 1959), and when leaves are treated withcompounds known to promote the functioning of plasma membrane ATPases(Mengel and Geurtzen, 1988). Leaf acid sprays could be potentially useful in somecrops to control chlorosis (Tagliavini et al., 1997). These and other data mayindicate that lowering the pH of the leaf apoplast could re-mobilize Fe (Kolesch etal., 1984; Mengel and Geurtzen, 1988). However, the specific mechanism responsiblefor the Fe immobilization in chlorotic leaves has not been elucidated and deservesfurther investigation.

ACKNOWLEDGMENTS

This work was supported by grants from the Dirección General de InvestigaciónCientífica y Técnica (PB 94-0086) and The Commission of European Communities(AIR-CT94-1973) to J.A. and from the Plan Nacional de Investigación (AGF94-0770) to A.A. F.M was supported by a contract from the Spanish Ministry forCulture and Education (MEC). Authors gratefully acknowledge the skillful technicalassistance of Aurora Poc in measuring chlorophyll, and Conchita Fustero andCarmen Lope with the mineral analysis.

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IRON CHLOROSIS PARADOX IN FRUIT TREES 825

Terry, N. and G. Low. 1982. Leaf chlorophyll content and its relation to the intracellularlocalization of iron. J. Plant Nutr. 5:301-310.

van den Driessche, R. 1978. Response of Douglas fir seedlings to nitrate and ammoniumnitrogen sources at different levels of pH and iron supply. Plant Soil 49:607-623.

Venkatraju, K. and H. Marschner. 1981. Inhibition of iron-stress reactions in sunflower bybicarbonate. Z. Pflanzenernähr. Bodenk. 144:339-355.

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