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Magnetic field affects meristem activity and celldifferentiation in Zea mays rootsM. B. Bitonti a , S. Mazzuca a , T. Ting b & A. M. Innocenti aa Department of Ecology, University of Calabriab Department of Chemistry, University of Calabria, Rende, Italy

Available online: 19 Aug 2006

To cite this article: M. B. Bitonti, S. Mazzuca, T. Ting & A. M. Innocenti (2006): Magnetic field affects meristem activity andcell differentiation in Zea mays roots, Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology,140:1, 87-93

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ECOLOGY AND ECOPHYSIOLOGY

Magnetic field affects meristem activity and cell differentiationin Zea mays roots

M. B. BITONTI1, S. MAZZUCA1, T. TING2 & A. M. INNOCENTI1

1Department of Ecology, University of Calabria, and 2Department of Chemistry, University of Calabria, Rende, Italy

AbstractExposure of Zea mays seedlings to a continuous electromagnetic field (EMF) for 30 h induced a 30% stimulation in the rateof root elongation compared with the controls. It also resulted in a significant increase of cell expansion, in both the acropetal(metaxylem cell lineage) and basipetal (root cap cells) direction. In addition, in EMF-exposed roots a precocious structuraldisorder was observed both in differentiating metaxylem cells and root cap cells. All these features may be consistent with anadvanced differentiation of root cells that are programmed to die. EMF treatment also resulted in a significant reduction inthe size of the quiescent centre in the root apical meristem. The extent to which these responses are causally linked isdiscussed.

Abbreviations: EMF: electromagnetic field; MES: 2-[N-morpholino]ethanesulfonic acid buffer; QC: quiescentcentre; RAM: root apical meristem

Key words: Magnetic field, metaxylem differentiation, quiescent centre, root cap, root meristem

Introduction

Sessile plants are very sensitive organisms to

evaluate the effects of environment on growth and

development. As a consequence, growth responses to

different exogenous stimuli have been widely inves-

tigated, especially in plant roots (Barlow &

Rathfelder, 1985; Okamoto & Tatara, 1995; Crook

& Ennos, 1996; Goodman & Ennos, 1996). Exposure

of humans, animals and plants to different levels of

electromagnetic field becomes a constant of current

life, due to ever increasing employment of electrical

and technological devices. Notably, even more

evidence has been accumulated showing that electro-

magnetic fields can affect living organisms (Jenrow

et al., 1995; Blank & Goodman, 2002; Piatti et al.,

2002; Hood, 2004).

In plants, the first evidence of the influence of

magnetic field on early growth processes dealt with

the induction of cress root curvature in the seed by a

static magnetic field (Audus, 1960). Later on,

Brulfert et al. (1985) and Inoue et al. (1985) showed

that the growth rate of seedlings could be altered

following exposure to low 60 Hz magnetic field, with

strength being from 70 to 48 mT respectively. Other

evidence demonstrated that changes in root tropism

induced by magnetic field were triggered by intracel-

lular displacement of amyloplasts in the statocytes of

root cap (Kuznetsov & Hasenstein, 1996; Kuznetsov

et al., 1999). More recently, the effects of either

continuous or pulsed magnetic field on plant growth

and development have been investigated in a large

number of plant species (Yano et al., 2001; Es’kov

& Darkov, 2003; Kalinin & Boshkova, 2003).

Generally, the effects of exposure to magnetic field

include the modulation of root growth rates, the

increase in wet and dry weight, the induction of

primary root curvature. By contrast, very little

information exists on the effects induced by magnetic

field at the cellular level (Inoue et al., 1985; Stange

et al., 2002).

With a view to providing some new insights into the

influence of electromagnetic fields on root growth, in

the present work we selected Zea mays, a species with

a very well characterized root apical meristem. It is

well known that following specific treatments such as

X-radiation, or prolonged exposure to low tempera-

ture, root growth is guaranteed through the activation

of cell division in the QC (Clowes, 1972; Rost &

Van’t Hof, 1973; Webster & Langenauer, 1973;

Correspondence: M. B. Bitonti, Dipartimento di Ecologia, Universita della Calabria, I-87030 Arcavacata di Rende (CS), Italy. Tel.: þ39 0984 492965.

Fax: þ39 0984 492964. E-mail: b.bitonti@unical.it

Plant Biosystems, Vol. 140, No. 1, March 2006, pp. 87 – 93

ISSN 1126-3504 print/ISSN 1724-5575 online ª 2006 Societa Botanica Italiana

DOI: 10.1080/11263500500511314

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Barlow & Pilet, 1983; Muller et al., 1994). Thus, our

attention was mainly drawn to verify the effects

of exposure to a continuous strong magnetic field

on the quiescent centre (QC) of the root apical

meristem. Moreover, laser-ablation studies on roots

of Arabidopsis thaliana, have clearly shown that QC

cells play a key role in root growth by suppressing

differentiation of those cells which lie on its surface

(Van der Berg et al., 1997) and consequently by

controlling vascular bundle repatterning (Sabatini

et al., 1999). Hence we have explored whether the

magnetic field affected the size of QC and the extent

to which such alteration might be linked to changes in

cell expansions, in both acropetal (metaxylem cell

lineage) and basipetal (root cap cells) direction, as an

index of the differentiation process.

Materials and methods

Growth conditions within the magnet cavity

Maize seeds (Zea mays L., Pioneer HI-Bred), pre-

viously sterilized in 3% NaClO, were germinated in

Petri dishes on moistened paper, at 25+ 0.58C in

the dark. Two-day-old seedlings with primary roots

that were about 8 mm long were transferred into vials

and maintained using a perfusion system (Figure 1a),

which was designed to provide continuous nourish-

ment to the seedlings within the cavity of a Bruker

MSL300 NMR spectrometer magnet. The seedlings

were oriented parallel to the 7 Tesla electromagnetic

field (EMF) (see Figure 1b).

Root elongation and mitotic activity

Seedlings were transferred to two vials (n¼ 18 per

vial) containing Mes buffer (10 mM Mes þ 0.2 mM

CaSO4, pH 6). One vial was exposed to EMF for

30 h in darkness. During exposure, roots were

perfused through the peristaltic pump with 2 L of

MES buffer, which was renewed every 10 h. The rate

of perfusion was calibrated in order to maintain a

temperature of 25+ 1.08C in the buffer inside the

vial. The control vial was placed vertically outside the

magnet cavity, in a growth chamber in exactly

the same conditions as described above. Every 10 h,

the length of both EMF-exposed and control roots

was measured. At each sampling time, three roots

were collected, fixed in ethanol:acetic acid 3:1 (v/v)

and the apices were squashed for mitotic index

analysis. Another three roots were fixed in 4%

gluteraldeides in phosphate buffer, embedded in

LR White’s resin and 3mm longitudinal sections of

the root tip (4 mm in length) were stained with

Coomassie Blue for histological analyses. Mitotic

index was estimated by scoring 150 nuclei for each

control and EMF-exposed root. For the histological

analyses, the size (mean area) of root cap cells, the

cell length and the cell number along the metaxylem

cell lineage were measured on median longitudinal

Figure 1. (a) Vial containing seedlings perfused through a peristaltic pump with recycling buffer inside and outside the vial; (b) seedling

orientation in the electromagnetic field. N: North pole of field.

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sections of each control and EMF-exposed root by

means of the NIH Image analysis system (National

Institute of Health, Maryland, US). The entire ex-

periment was replicated three times.

Continuous label (CL) with 3H-TdR for QC

visualization

CL was carried out in the EMF and control treatments

by exposing eight seedlings to an oxygenated solu-

tion of tritiated thymidine ([methyl-3H]thymidine,

925 Gbq mmol71, 9.25 104 Bq cm73) in 10 mM MES

for 30 h. Three different replicate experiments were

carried out. At the end of each CL treatment, the

length of both EMF-exposed and control roots

was measured, thereafter the roots were fixed in

ethanol:acetic acid 3:1 (v/v). For the quiescent centre

measurements, the roots (n¼ 4 for each replicate) of

both EMF and controls were wax-embedded and

sectioned longitudinally at 7mm. Sections were

Feulgen stained after hydrolysis in 1M HCl at 608Cfor 7 min and thereafter autoradiographed using Ilford

L4 emulsion diluted 1:1 (w/v) with a 1-month

exposure time. The size of quiescent centre (QC)

was measured from median longitudinal sections as

described by Feldman & Torrey (1975); roots (n¼ 12)

from the different replicates were analyzed and the

number of cells in the QC estimated by scoring the

most median longitudinal sections.

Results

Root length and mitotic activity

Following the selection of primary roots that were

about 8 mm long, the initial aim was to establish

whether or not EMF affected root elongation and

mitotic activity. As shown in Figure 2, the roots of

seedlings exposed to EMF were significantly longer

than the controls at each sampling time (p5 0.001).

The rate of root elongation in EMF-treated roots was

significantly faster (1.21 mm h71) than in the con-

trols (0.95 mm h71). Comparable differences in root

elongation between exposed and control roots were

detected in samples exposed to CL, the average

difference being 28% after 30 h EMF exposure (data

not shown). The exposure to the EMF also affected

the mitotic activity of root meristems. In fact, in roots

exposed to the EMF the mitotic index was 8.5+ 0.5,

significantly higher (0.0015 p5 0.01) than the

control roots (7.0+ 0.3).

Size of the QC following 30 h CL with 3H-TdR

The QC of root apical meristems (RAM) was

visualized by the standard technique of continuous

labelling (CL) with 3H-TdR. In roots exposed to

EMF, the QC is significantly smaller than the

controls whether judged by height or width in

longitudinal median sections (Table I). These data

are supported by micrographs of the QC in both

treatments (Figure 3). We did not observe differ-

ences in cell size between treatments and, therefore,

cell number is also significantly smaller in QCs

sampled from the EMF treatment compared with the

controls. However more labelled cells were observed

in the QCs of roots exposed to EMF.

Cytological analysis in root cap and metaxylem cells

The mean area of root cap cells was measured at 10

and 30 h of treatment in both EMF and control roots

(Table II; Figure 4). After 10 h of exposure to EMF

cell size was not affected, while a significant increase

(21.4 %) in cell area was observed following pro-

longed treatment (30 h exposure), starting from the

root junction to the cap end. Moreover, following

the EMF exposure few and small statocytes were

observed in the columella cells as compared

Figure 2. The rate of root elongation (mm) in maize seedlings

during 30-h exposure to the magnetic field (black squares) and in

control seedlings grown outside of the magnet cavity (white

squares). Values are the mean+SE of three replicates; p5 0.001

at each sampling time, except t¼0). For control roots

y¼7.46þ 0.956x, R2¼0.997; for treated roots y¼6.73þ 1.213x,

R2¼ 0.990.

Table I. The size and cell number of the QC together with the

labelling index (LI) within the quiescent centre in roots of maize

exposed to electromagnetic field (EMF) for 30 h, as compared

with the control.

Test

Height

(mm)

Width

(mm) cell number LI (%)

EMF 111+10* 231+ 12** 303+ 27** 5+ 1.1**

Control 125+11* 342+ 15** 520+ 70** 2+ 0.2**

Values are the mean+SE of measurements on roots (n¼12) from

three different replicates. *p5 0.01; **p5 0.001.

Magnetic field-induced changes to maize root 89

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to control roots, indicating that both structural

and functional disorder was occurring (compare

Figure 4c with 4d).

Cell length was measured along a metaxylem cell

lineage at 10 and 30 h in both the EMF and control

treatments (Figure 5). At 4,000 mm from the junction

between RAM and root cap, metaxylem cells were

significantly longer in the EMF if compared with

control treatment at 30 h (p5 0.001) and a lesser

but nevertheless significant difference occurred in

roots sampled at 10 h (Figure 5a). Clearly the magni-

tude of the differences between treatments at these

sampling times is consistent with the differences

between root lengths at these times (Figure 2 cf.

Figure 5a). Comparison between metaxylem cell

lengths at shorter distances from the RAM revealed

the first significant difference between treatments at

300 mm in root sampled at 30 h ( p5 0.002) but not

in those sampled at 10 h ( p5 0.05). In the latter

roots, significant differences between treatments

were first detected in metaxylem cells at 800 mm.

However at both sampling times metaxylem cell

length was progressively longer in the EMF com-

pared with the control treatment. Hence, the

magnitude of difference between treatments (greater

at 30 h compared with 10 h), and the position along

the metaxylem lineage that cell length differences

could first be detected (800 mm at 10 h, 300 mm at

30 h) are consistent with the differences in root

length between treatments. The difference in metax-

ylem cell length between treatments is well illustrated

in Figure 6. In the EMF treatment (Figure 6a),

the metaxylem cell was much longer that a com-

parable metaxylem cell in the control (Figure 6b). In

addition, metaxylem cells in the EMF treatment

exhibited nuclei with highly condensed chromatin

and an incipient structural disorder became evident.

In both exposed and control roots, cell number

along the metaxylem lineage was also evaluated,

starting at 100 mm until 4,000mm from root cap

junction. After 10 h of exposure to EMF, metaxylem

cell number was 58.0+ 0.7, whereas in control roots

the cell number was 62.0+ 1.0. In the same length

interval, the cell number dropped to 27.0+ 0.5 and

31.0+ 0.3 in roots exposed to EMF for 30 h and in

control roots respectively. As a result, about three

more cells were detected along the metaxylem cell

Figure 3. Autoradiographs of median longitudinal sections of

maize roots following methyl-3H-thymidine continous labelling.

(a) root after 30-h exposure to the magnetic field; (b) control root

with a prominent quiescent center in the apex. The absence of

labelling together with the dotted ring indicates the upper and

lower boundary of the QC. The arrow indicates three cells escaped

from the QC. Scale bar: 70mm.

Table II. The mean area, expressed as mm2, of root cap cells in

seedlings of maize exposed to electromagnetic field (EMF) for 10

and 30 h, as compared with the control.

Test 10-h exposure 30-h exposure

EMF 243+ 13 393+25*

Control 258+ 16 255+18*

Values are the mean+SE of measurements on roots (n¼9) from

three different replicates. *p50.001.

Figure 4. Microphotographs of root cap cells starting from the

junction to the root meristems (a, b) and in the distal zone of

columella (c, d) in the control (a, c) and after 30-h exposure to the

magnetic field (b, d). Scale bar: 15mm.

90 M. B. Bitonti et al.

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lineage in control roots with respect to those exposed

to the EMF.

Discussion

Our data are consistent in showing that a strong

electromagnetic field stimulated primary root elon-

gation in Zea mays seedlings. This finding is in

agreement with the stimulation of growth processes

induced in other species following exposure to con-

tinuous EMF (Davies, 1996; Yano et al., 2001;

Es’kov & Darkov, 2003; Kalinin & Boshkova, 2003).

Root growth is dependent upon cell reproduction

in the root meristem and subsequent elongation and

differentiation of the descendant cells (Webster &

MacLeod, 1980, 1996; Beemster & Baskin, 1998).

The rise of mitotic index in the RAM of Zea

seedlings exposed to EMF is consistent with either

a stimulation of cell proliferation or an extension of

mitotic phases relative to interphase duration in-

duced by EMF. Hence, measurements of cell cycle

length required to resolve the contribution of cell

division to EMF-induced increases in root length are

worthy of further investigation.

Notably, in the primary root apices of Zea seed-

lings, substantial differences in cell size were induced

following the exposure to the EMF. Root cap cells

were significantly larger and metaxylem cells were

significantly longer starting from the quiescent centre

boundary compared with the controls. This latter

result is consistent with three cells less along the

metaxylem cell lineage in the first 4 mm from the

root cap junction found in the EMF exposed roots.

In our view, the EMF-induction of longer metaxylem

cells is an important component of the EMF-

induced increase in the rate of root elongation.

In the metaxylem cells the effect of EMF was

particular evident from 800 to 1,200 mm. In maize

Figure 5. Mean metaxylem cell length (mm) at different distances

from the junction between the tip of the root meristem, and the

root cap in roots exposed to the magnetic field (gray bars) for

(a) 10 h and (b) 30 h or in comparably sampled control roots

(white bars). Values are the mean+SE of three replicates (n¼16;

p50.002 from 300mm to 400 mm; p5 0.001 from 500 to

4,000mm).

Figure 6. Longitudinal sections of metaxylem cells at 800mm from

the junction between the tip of the root meristem and the root cap

(a) after 30-h exposure to the magnetic field and (b) in the control.

Arrow showing the nucleus with highly condensed chromatin in

exposed roots. Scale bar: 15mm.

Magnetic field-induced changes to maize root 91

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roots, this zone corresponds to the ‘distal elongation

zone’ characterized by cells that are strongly involved

in the response of roots to a variety of environmental

stimuli (Erickson & Sax, 1956; Ishikawa & Evans,

1995). In this context, intrinsic electric fields have

been found around the root tip (Behrens et al.,

1982, 1985; Ryan et al., 1990; Weisenseel & Meyer,

1997). These minute electric currents seem to be

related to the polar transport of endogenous auxin

in the root tissue (Biro et al., 1982; Lee et al., 1984;

Behrens et al., 1985) and to the cytosolic changes

of Ca2þ. Since both auxin and Ca2þ regulate the

rate of cell expansion (Behrens et al., 1982, 1985;

Lee et al., 1983; Pickard, 1985), our hypothesis is

that EMF may disrupt the pattern of intrinsic ionic

currents by altering the ion movement across the

plasma membrane (Stange et al., 2002), thus altering

the elongation of exposed roots.

The experiment of CL clearly showed that the size

of QC was substantially reduced in the RAM of roots

exposed to EMF with three layers of cells escaping

from QC control. This reduction in QC size, may

have resulted in precocious expansion and differ-

entiation of contacting cells in both basipetal (root

cap) and acropetal (metaxylem lineage) direction. In

fact, in exposed roots the early differences in length

(at 300 mm from 4,000mm) of metaxylem cells were

accompanied by a precocious structural disorder.

Analogously, symptoms of a precocious structural

and functional disorder were observed in the

sloughing cells of the root cap, which exhibited

small statocytes, likely as a consequence of starch

degradation induced by stress imposed by strong

EMF-exposure. Notably, rapid degradation of

amyloplasts in columella cells has been detected

also in water-stressed roots showing a reduced

responsiveness to gravity (Takahashi et al., 2003).

Thus, features described for both metaxylem and

root cap cells may be consistent with an adv-

anced differentiation of cells that are programmed

to die.

Given that QC cells repress differentiation in

contacting apical initial cells (Van der Berg et al.,

1997; Sabatini et al., 1999) we suggest that the onset

of cell differentiation was permitted to occur closer

to the root tip in the EMF, because of cells escaping

from QC control. In conclusion, we have demon-

strated that EMF results in an increase in primary

root elongation, and the onset of metaxylem cell

elongation occurs at a closer distance to the root tip

than in control. The quiescent centre in the RAM

was significantly smaller in the MF compared with

the control treatments. The precocious elongation of

the metaxylem cells and the reduction in QC size

may be casually linked but verification will depend

on experiments that focus on the onset of differ-

entiation in response to MF.

Acknowledgment

This work was funded by the University of Calabria

(ex 60% grant).

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