boron behavior in apple plants in acidic and limed soil

2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.plant-soil.com

J. Plant Nutr. Soil Sci. 2013, 176, 267–272 DOI: 10.1002/jpln.201100366 267

Boron behavior in apple plants in acidic and limed soilVasileios Antoniadis1*, Christos Chatzissavvidis2, and Asterios Paparnakis2

1 Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Fytokou Street, Volos, GR-384 46, Greece2 Department of Agricultural Development, Democritus University of Thrace, Pantazidou 193, Orestiada, GR-621 00, Greece

AbstractIn dry Mediterranean-type climates boron (B) levels may naturally be high and even toxic toplants. Although liming of an acidic soil is expected to decrease B levels, it is not known whatthe effects would be in such areas of high-B soils, especially in B-sensitive crops such as appletrees. Thus, our aim was to study the behavior of added B in newly planted apple rootstocks inan acidic soil which was limed to pH 6.5 in an outdoor pot experiment. Added B increased signifi-cantly B extractability from soil, and B levels were lower in the limed compared to the acidic soils.Plant B concentrations also increased with added B but differences between limed and unlimedsoils were not evident, because plant B did not seem to reflect changes in B behavior in soil.However, B uptake was significantly increased with added B, and was further increased with lim-ing, contrary to what the soil extractions indicated, due to improved growth conditions. Ourresults show that although liming decreased soil B levels, at the same time it did not affect plantB concentration and accelerated the uptake of added B, indicating a possibility for increasedsoil-to-plant mobility of B.

Key words: Malus domestica / extractable boron / boron translocation / boron uptake

Accepted January 1, 2013

1 Introduction

Boron (B) is an essential metalloid element with well-recog-nized physiological functions in plants, which include sugartranslocation through cell membranes and a critical role innucleic acid metabolism. Boron is particular in its behavior insoil because the range between deficiency and toxicity is nar-row (Bell, 1997). This means that plants in B-deficient soilsmay exhibit toxicity symptoms if soils are overfertilized withB. Although there is a good number of published work con-cerning B nutrition of plants, most of these publications dealwith the problem of B deficiency (e.g., Yu and Bell, 2002).The reason is that such studies are typically based in areaseither with high rainfall (Fageria et al., 2007) or with tempe-rate climates (Stevens and Dunn, 2004). However, underMediterranean climatic conditions (dry and warm during thegrowing seasons of most of the high-value crops), and whererainfall is not sufficient to leach the element from the rootzone, B tends to accumulate and in many cases to exceedtoxic levels. Also in such areas, irrigation water is often highin B (Dionysiou et al., 2006). For example, in northernGreece, well water with high B concentration has been usedfor irrigation of kiwifruit and olive orchards (Chatzissavvidiset al., 2004), although in that particular work, no toxicitysymptoms were observed in the studied olive cultivars. Thus,in warm and dry environments, B deficiency is less likely thantoxicity, but this problem has not been adequately addressed.

Boron behavior in soil depends on soil properties, of whichpH is the single most important factor. It is commonly be-lieved that (1) in acidic soils (mainly with pH < 6), B is lea-ched along with base cations (Jiang et al., 1999) and that (2)B adsorption increases with increasing pH up to a value of

9.2 (as observed in batch sorption tests, e.g., Karahan et al.,2006). These two points have repeatedly been observed invarious studies (e.g., among others Krug et al., 2011; Tsadi-las et al., 2005), but may not necessarily be valid in dry acidicMediterranean-type soils. In those areas, even acidic soilsmay have high B levels due to continuous additions (e.g., irri-gation water, as indicated earlier) and thus, there is a void inknowledge on whether liming can reduce B levels sufficientlyto prevent plant toxicity. Moreover, even if plant B concentra-tions decrease with liming, plant biomass is expected toincrease. Thus, the effect of liming on B uptake (the productof B concentration and biomass) is not known in high-B soils.

Particularly apple (Malus domestica Borkh.), a wide-spreadand high-profit tree cultivated in the Mediterranean, typicallyhas high B requirements (Wojcik and Treder, 2006). Newlyestablished apple plants tend to be especially sensitive tochanges in B availability. This is related to the mobility of Bthrough phloem in apple, which does not usually occur inother species, since B is generally considered “to have lim-ited phloem mobility in higher plants” (Brown and Hu, 1996).Yet, apple plants have not been tested in high-B soils.Research on apple plants emphasizes B deficiency (e.g.,among others Wojcik et al., 2008; Wojcik, 2000; Neilsen et al.,2004) and thus, the effects of liming on B solubility, on plant Bconcentrations, and on B uptake are not known. In an attemptto test the hypothesis that liming is a measure to reduce Btoxicity in apple trees, we aimed at evaluating soil extractableB, as well as B concentrations and B uptake by apple plantsin an acidic and limed soil with high B values elevated by Badditions.

* Correspondence: Dr. V. Antoniadis; e-mail: [email protected]

2 Material and methods

The soil we used was collected from the 0–20 cm layer andwas obtained from Patagi, near Orestiada, North Greece. Itwas a Typic Rhodoxelalf, silt loam (41% sand, 8% clay), with1.2% organic C, 0.60 dS m–1 electrical conductivity (1:5H2O), 5.8 and 0.75 g kg–1 dithionite-extracted Fe oxides andAl oxides, respectively, and pH 4.2 (1:2.5 H2O). The soil wasair-dried and sieved through a 2 mm sieve. A portion of it wasthoroughly mixed with lime (calcitic marble quarry tailings,with 80% CaCO3 and insignificant B content, sieved though a1 mm sieve) at a rate of 0.64 g of lime per kg of soil, equiva-lent to 2 t CaCO3 ha–1 assuming a field bulk density 1.33 gcm–3 and a 30 cm depth of lime incorporation. The quantity ofthe applied lime was predetermined in a preliminary incuba-tion test, where this lime was applied at several rates to 100 gsamples of the same soil and the pH values recorded after 1week. Based on this test, the above mentioned quantity oflime to raise the pH to the target value of 6.5 was determined.Exchangeable Ca2+ was 1.323 cmolc (kg soil)–1 for the acidicand 2.347 cmolc (kg soil)–1 for the limed soil, which confirmsthat liming added 1.024 cmolc CaCO3 kg–1 equal to 512 mgCaCO3 kg–1 or 2.05 t CaCO3 ha–1.

A quantity of 1.95 kg of soil was placed in 40 5 L plastic pots(20 of which contained the acidic and 20 the limed soil) andwas mixed with perlite at a 1:1 ratio for better aeration andwater retention and movement. Two-year-old apple (Malusdomestica cv. Redchief) plants budded on MM106 rootstockwere placed in each pot (one plant per pot). From the pots nodrainage was allowed. Any water leached from the pots wascollected in individual pot dishes and was given back into thepots. The experiment took place in Orestiada, Greece(26°32′04.69″ E, 41°30′35.84″ N, 41 m altitude) under ambi-ent climatic conditions (Tab. 1).

The experiment commenced on May 9, 2009. In addition tonormal rainfall, plants received 500 mL of drip-irrigation water,applied every 2 d (for comparison, this was equal to 1237 mmon an area basis), and were left to equilibrate for 6 weeks,during which time growth commenced. After that, B wasadded to the pot surface at the levels of 0 (B-0), 1 (B-1), 3 (B-3), and 5 (B-5) mg (kg soil)–1 (equivalent to 0, 2, 6, and 10 kgB ha–1), and each treatment was replicated five times at each

lime level. In week 8, from the establishment of the plants(2 weeks after the addition of B) soil and leaf samples werecollected from each treatment. Soil samples from each potwere collected from three different locations with a plasticspatula from immediately below the soil surface and wereincorporated into one composite sample per pot. One pair offully developed leaves from the 4th or 5th node from the topof main shoots was used for analysis. A second leaf and soilsamples were also obtained at the end of the experiment, onSeptember 13, 2009 (or 11 weeks after B additions) using thesame soil methods. At that time, the plants were uprootedand separated into various parts (roots, stems, leaves).

The soil samples were extracted for soluble B with hot 0.01 MCaCl2 (1:2 soil-to-solution ratio, boiled for 10 min, Datta et al.,1998). Leaf, stem, and other plant samples were washedwith deionized H2O, dried for 48 h (or until no further loss inweight was recorded) in a forced-draught oven, weighed, andground in a mill to a fine powder. A 0.5 g subsample of theground plant parts was weighed into porcelain crucibles andashed at 500°C for 5 h. The ash was extracted with 20 mL20% HCl (Jones et al., 1990). In each plant extract (as wellas in the soil filtrates), B was measured colorimetrically viathe azomethin-H method (Wolf, 1971) in a spectrophotometerat 420 nm. From the various plant parts, whole-plant B con-centration was estimated as the weighted average of all plantsamples. Apart from B concentration in each plant part, Buptake was also determined (expressed in mg of plant Bpot–1), as the product of B concentration in plant (mg of plantB [kg plant]–1) and plant dry-matter weight (g of plant pot–1).The percentage of B recovery was also determined as fol-lows:

Recovery (%) = (B uptake in treatment – B uptake in zeroadded B control) × 100 / B added in soil.

Factorial ANOVA (with the two factors being liming and Brate) was undertaken on all experimental data, and differ-ences between treatments were compared according to theLSD test for a level of significance of 95% (p < 5%). In thefigures, the error bars represent the standard error of themean of each treatment. Also in the figures, treatments thathave the same letters represent groups within which valuesare not statistically different at the level of 95%, according toDuncan’s multiple range test. Asterisks indicate the signifi-cance of differences between identical treatments in themeasurements that we obtained over time. The statisticalpackage used was Statgraphics Plus 2.1 for Windows.

3 Results

3.1 Boron in soils

In week 8, B extracted from control soils was in the expectedrange for high-B soils (between 1 and 2 mg kg–1), with no dif-ference between B in the acidic and the limed soil (Fig. 1A).Added B significantly increased extractable B levels in theacidic soil (at B-3 and B-5, B was significantly different fromthe control), as it was for the limed B-5 treatment. In week 17,the extractable levels decreased significantly compared to


Table 1: Selected climatic conditions during the experimental period,2009, near the experimental site. The data were obtained from theNational Meteorological Service of Greece.

Meantempera-ture/ °C

Meanmaximumtempera-ture/ °C

Meanminimumtempera-ture/ °C

Rainfallheight/ mm

Dayswithrain

May 20.2 28.0 12.4 27.4 3

June 24.1 31.9 15.5 46.3 7

July 26.9 34.0 19.0 40.6 2

August 25.3 33.4 17.7 33.0 1

September 20.1 26.1 14.1 106.9 5

268 Antoniadis, Chatzissavvidis, Paparnakis J. Plant Nutr. Soil Sci. 2013, 176, 267–272

week 8 in the acidic B-5, and there were no differencesamong treatments (except for the limed B-5, which increasedcompared to B-0, Fig. 1B).

3.2 Boron concentration in plants

Boron concentration in apple leaves was above 60 mg kg–1 inthe control treatment in the early sampling time (week 8,Fig. 2A). In both acidic and limed soils, added B at B-3 andB-5 increased B concentrations in leaves compared to thecontrol. In the second sampling time (week 17, Fig. 2B), Bconcentrations decreased significantly in all treatments, evenin the plant leaves grown in the control soils. As a result, onlyin the limed soil B concentration was higher at B-5 comparedto the control, while in all the other treatments there were nodifferences from the control. In stems (end-of-the-experimentsampling only, Fig. 2C), B levels in the acidic soil were higherthan those in the limed soil at B-3 and B-5, while B-0 and B-1were similar in acidic and limed soils, indicating an interactionof B rate and liming. Stem B concentrations also increasedsignificantly with B additions in the acidic soil (with the orderbeing B-5 > B-3 > B-1 = B-0), while in the limed soil only B-5was higher than the control. When B concentration in thewhole plant was taken into consideration, B levels were lower


(A)d

b

aa

c

aaa

0

1

2

3

4

B-0 B-1 B-3 B-5

Week 8

B /

mg k

g–

1

(B)

ab*ababab

bab

aba

0

1

2

3

4

B-0 B-1 B-3 B-5

Week 17

B /

mg k

g–

1

Acidic

Limed

Figure 1: Hot CaCl2–soluble B at two sampling times (A and B) asaffected by B-application rate and liming (B-0: no added B; B-1: 1 mgB kg–1; B-3: 3 mg B kg–1; B-5: 5 mg B kg–1). Error bars representstandard errors of the means of each treatment. Treatments withidentical letters represent groups within which values are notsignificantly different at the 95% level. Asterisks indicate thesignificance of differences at the 95% level between identicaltreatments in the measurements obtained over time.

Fig.2

(A)bc

bc

aa

c

bcab

a

0

20

40

60

80

100

120

140

B-0 B-1 B-3 B-5

Leaves-Week 8

B /

mg

kg

–1

(B)

ab* ab*ab*

b*

a*a*

a*

b*

0

20

40

60

80

100

120

140

B-0 B-1 B-3 B-5

Leaves-Week 17

Whole plant

b b b

c

a

bbc

c

0

10

20

30

40

50

60

B-0 B-1 B-3 B-5

(D)

Acidic

Limed

(C)

ab ab

c

d

aa

ab

c

0

20

40

60

80

B-0 B-1 B-3 B-5

Stems

B /

mg

kg

–1

B /

mg

kg

–1

B /

mg

kg

–1

Figure 2: Boron concentrations in apple-plant leaves attwo sampling times and in stems and whole apple plantsat the end of the experiment as affected by B-applicationrate and liming. Error bars represent standard errors ofthe means of each treatment. Treatments with identicalletters represent groups within which values are notsignificantly different at the 95% level. Asterisks indicatethe significance of differences at the 95% level betweenidentical treatments in the measurements obtained overtime.

J. Plant Nutr. Soil Sci. 2013, 176, 267–272 Boron in apple plants 269

than B in leaves alone (Fig. 2D). Also, plant B concentrationwas significantly higher in the control acidic soil than B in thecontrol limed soil. Added B at B-5 increased significantly Bconcentrations in plants of both acidic and limed soilscompared to the control, but there were no differences be-tween plants from the acidic and the limed soil (when identi-cal B treatments are compared).

3.3 Dry matter

Dry-matter weight of leaves was significantly increased atB-3 and B-5 compared to B-0 with added B in the acidic soil,while in the limed soil leaf dry matter was not significantly dif-ferent in the various B treatments (Fig. 3A). In the stem dry-matter weight, there was a significant increase in the limedcontrol compared to the acidic control, but there was nofurther increase with added B in either soil (Fig. 3B). Similarfindings for the whole-plant dry-matter weights (Fig. 3C) indi-cated where there was a significant increase with liming. Inthe acidic soil, B-3 was higher than B-1 and the control, whilein the limed soil there was no difference between any of thetreatments.

3.4 Boron uptake

Boron uptake from the control acidic soil was not differentfrom the limed control (Tab. 2). In both limed and acidic soils,B uptake significantly increased with added B. The percen-tage of B recovery at B-5 was lower than at B-1 in the acidicand limed soil. Boron recovery increased with liming whenthe same B additions are compared (except for B-5, which

was not different from the acidic B-5 recovery), indicating aninteraction of lime and B-rate treatments.

4 Discussion

Liming in the form of CaCO3 of an acidic soil decreases totalacidity due to a twofold effect: First, added Ca2+ graduallysubstitutes for clay interlayer Al polymers, forcing them intosoil solution, and, second, added CO2�

3 and HCO�3 ions

reduce active acidity, increasing soil solution pH. As a resultof the increased solution pH, previously fixed Al polymerscannot stay dissolved in solution, and precipitate as insolubleAl(OH)3 (Essington, 2004, p. 473). Thus it would be expected


Fig.3

(A)bc

c

abc

a ababcabcabc

0

2

4

6

8

B-0 B-1 B-3 B-5

Leaves

g p

ot–

1

(C)

aa

b abb ab ab

b

0

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120

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B-0 B-1 B-3 B-5

Whole plant

Acidic

Limed

(B)

a a

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bab

ab ab

0

5

10

15

20

25

30

B-0 B-1 B-3 B-5

Stems

g p

ot–

1g p

ot–

1

Figure 3: Dry-matter yield of leaves, stems, and wholeplant at the end of the experiment as affected by B-application rate and liming. Error bars represent standarderror of the mean of each treatment. Treatments withidentical letters represent groups within which values arenot significantly different at the 95% level. Asterisksindicate the significance of differences at the 95% levelbetween identical treatments in the measurementsobtained over time.

Table 2: Boron uptake by the whole apple plant and percentage Brecovery (uptake relative to that added) at different B rates in both thelimed and the acidic soil. Different letters within each treatmentsindicate significant differences between means at the p < 5% level.

Added B B uptake Recovery

/ mg kg–1 / mg pot–1 / mg pot–1 / %

Acidic 0 0 1.47 a –

1 1.95 2.07 b 30.6 bc

3 5.85 2.86 c 23.7 a

5 9.75 3.72 e 23.1 a

Limed 0 0 1.46 a –

1 1.95 2.18 b 37.4 d

3 5.85 3.39 d 33.1 c

5 9.75 4.20 f 26.1 ab


that liming even in the control soil could decrease B concen-trations (both in soil and plant), due to increased adsorptionof the B(OH)3 species (which predominates at pH < 9.2) ontothe freshly precipitated Al(OH)3 surfaces (as suggested byHavlin et al., 2005, p. 278). In this study, liming in the una-mended control treatments did not seem to have an effect oneither soil extractable B or on B concentrations in applestems and leaves. However, B concentration in whole plants(consisting of aerial parts as well as roots) for control treat-ments exhibited the expected decrease with liming. This maymean that stems would have reflected the past history of Bnutrition, rather than current soil-B availability changes, sinceplants were 2 years old when planted. Also, stem and leaf Bconcentrations may not have reflected the difference in Bchemical behavior in soil, because of the time needed for Btranslocation to stems and leaves. This was also suggestedby Matsi and Keramidas (1999), who limed acidic soils withfly ash and increased pH from 4.7 to 7.7. With this material,they added minimal amounts of B, as low as 0.15 mg (kgsoil)–1, insignificant even compared to the B-1 treatment ofthis study, and found no differences either in the B concentra-tions in the aerial parts of ryegrass or in hot water–extractableB between acidic and limed soils. Although this occurred inthe control, in the high-B additions liming showed theexpected trend, since at B-3 and B-5, B in the acidic soil washigher than in the limed soil (Fig. 1A), indicating an interactionof B rate and liming. This discrepancy in B behavior (B in con-trol vs. added B), as indicated in the soil extractions, seemsto suggest that added B is likely to have a different chemicalbehavior than indigenous B. The former is less stronglybound onto soil colloid surfaces, thus, it is more mobile insoil, and consequently more likely to be affected by liming.Indigenous B, even in acidic soils, is more strongly boundonto, or infused over time into, less mobile soil colloid regions(Goldberg and Suarez, 2011), thus, liming did not particularlyaffect native B in an adverse manner.

Upon B treatment, the increase in soil extractable-B levelswas evident in both the acidic and the limed soils at B-5 atweek 8 (Fig. 1A; as also found by Redd et al., 2008). Such anincrease with added B was also observed in the leaf B con-centrations (Fig. 2A). It is noteworthy, however, that, althoughsoil B concentration in the control was relatively high, withadditional B treatment leaf B concentrations did not reach thetoxicity threshold of 200 mg kg–1 (Brady and Weil, 2002,p. 640). It must be added that according to other studies, toxi-city symptoms (typically including decreased leaf chlorophyll,altered metabolism, and necrosis of mature tissues, accord-ing to Reid et al., 2004) may be observed at apple leaf B con-centrations of as low as 70 mg kg–1 (Neilsen and Neilsen,2003, p. 294), a level which was observed even at B-1(Fig. 2A). However, in our study there were no visual toxicitysymptoms for any treatment.

As for the observed decrease in leaf B over time, weattempted to explain it in terms of the reported phloem mobi-lity of B within some species, such as apple (Brown andShelp, 1997), which leads to B translocation from leaves tostems. Stem B concentration should have increased as thedifference in leaf B concentration between week 8 and week17 was enhanced. Thus, in order to quantify the possibility of

B translocation from leaves to stems, we conducted a corre-lation analysis between the difference in leaf B concentra-tions in weeks 8 and 17 vs. stem B concentration. The gener-ated relationship was negative and significant at p < 5% withR2 = 0.271 (Fig. 4), showing that there is some evidence tosupport that B was translocated from leaves and stored instems.

Although the increases in plant B concentrations, as well asthat of dry-matter weights, with added B were observed onlyin some B treatments, B uptake by plants increased signifi-cantly as B increased, indicating a significant interactionwhich dominated the two studied main effects. It is note-worthy that in the limed soil, B uptake was significantly higherthan that in the acidic soil, at B-3 and B-5 (at B-1 and in thecontrol, the differences were not significant), while B concen-trations in both plant (in all studied parts, except for B-3 andB-5 in stems, and B-0 in whole plant) and soil did not exhibitthis trend. This seems to be associated with the improvedgrowth conditions (including increased number of leaves,length of shoots, and total chlorophyll content, data notshown) that were established with liming, which in turnimproved absorption of B by the plant.

Increased B uptake, although not directly linked with B con-centration and thus B toxicity, may cause significant adverseeffects over time. Many researchers have used uptakeinstead of concentration as a possibility to indicate develop-ing B toxicity. For example, Paull et al. (1992) concluded that“tolerance [in the high B treatments] is attributable to variationin the uptake of B,” a finding also reported by Nable et al.(1990). Thus, increased uptake does indicate a possibility forincreased mobility of B, and thus, sensitive genotypes maybe adversely affected.

As a result of the observed B-uptake trends, B-recovery per-centage was significantly higher in the limed than in the acidicsoil (with the exception of the high B level, B-5, becauserecovery decreased with B additions whether limed or not).The B-recovery values were similar to that reported in otherstudies. For example, Boaretto et al. (2011) found a 21%recovery in a citrus-tree experiment, where B was added tothe soil with a nutrient solution. The percentage of B recoveryalso decreased with added B, an expected trend for bothmacro- and microelements (Dwivedi et al., 1992), indicating


R2 = 0.271*

p = 0.013

0

20

40

60

80

–100 –80 –60 –40 –20 0

(B leaf concentration) / mg kg–1

B s

tem

con

centr

atio

n /

mg k

g–

1

Figure 4: Correlation between the difference over time of leaf Bconcentration (week 8 leaf B concentration minus week 17 leaf Bconcentration) vs. stem B concentration. Asterisk indicates sig-nificance of correlation at the level of p < 0.05.

J. Plant Nutr. Soil Sci. 2013, 176, 267–272 Boron in apple plants 271

that plant efficiency to utilize soil available B decreases withincreasing B additions, and this functions as a plant mechan-ism to mitigate possible B toxicity.

5 Conclusions

With liming decreased B concentrations in apple plants wererecorded only in stems at B-3 and B-5, while B in leaves wasunaffected and whole-plant B decreased only at B-0. Thisindicates that in high-B soils, liming may not be a completelysufficient agronomic measure to reduce high B levels in appleplants. Boron uptake by apple plants increased significantlywith liming, probably due to improved growth conditions thatpositively affected plant biomass. Our results show that inhigh-B soils (such as those used here, i.e., acidic soils fromdry Mediterranean areas) liming may not reduce available-Blevels sufficiently, while, at the same time, it may trigger anacceleration of B uptake, an effect that over time may causeadverse effects to B-sensitive high-value crops such as appleplants.

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boron behavior in apple plants in acidic and limed soil

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