Review Article Plant Responses to High Frequency...

Review ArticlePlant Responses to High Frequency Electromagnetic Fields

Alain Vian1 Eric Davies2 Michel Gendraud3 and Pierre Bonnet45

1Universite drsquoAngers Campus du Vegetal UMR 1345 IRHS CS 60057 SFR 4207 QUASAV 49071 Beaucouze Cedex France2Department of Plant and Microbial Biology North Carolina State University PO Box 7612 Raleigh NC 27695 USA3Universite Blaise Pascal 24 avenue des Landais 63177 Aubiere Cedex France4Institut Pascal Universite Blaise Pascal BP 10448 63000 Clermont-Ferrand France5CNRS UMR 6602 63171 Aubiere France

Correspondence should be addressed to Alain Vian alainvianuniv-angersfr

Received 25 November 2015 Accepted 17 January 2016

Academic Editor Yan-Bo Hu

Copyright copy 2016 Alain Vian et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

High frequency nonionizing electromagnetic fields (HF-EMF) that are increasingly present in the environment constitute agenuine environmental stimulus able to evoke specific responses in plants that share many similarities with those observed after astressful treatment Plants constitute an outstanding model to study such interactions since their architecture (high surface areato volume ratio) optimizes their interaction with the environment In the present review after identifying the main exposuredevices (transverse and gigahertz electromagnetic cells wave guide and mode stirred reverberating chamber) and general physicslaws that govern EMF interactions with plants we illustrate some of the observed responses after exposure to HF-EMF at thecellular molecular and whole plant scale Indeed numerous metabolic activities (reactive oxygen species metabolism 120572- and120573-amylase Krebs cycle pentose phosphate pathway chlorophyll content terpene emission etc) are modified gene expressionaltered (calmodulin calcium-dependent protein kinase and proteinase inhibitor) and growth reduced (stem elongation and dryweight) after low power (ie nonthermal) HF-EMF exposure These changes occur not only in the tissues directly exposed butalso systemically in distant tissues While the long-term impact of these metabolic changes remains largely unknown we proposeto consider nonionizing HF-EMF radiation as a noninjurious genuine environmental factor that readily evokes changes in plantmetabolism

1 Introduction

High frequency electromagnetic fields (HF-EMF ie fre-quencies from 300MHz to 3GHz wavelengths from 1mto 10 cm) are mainly human-produced nonionizing electro-magnetic radiations that do not naturally occur in the envi-ronment excluding the low amplitude VHF (very high fre-quency) cosmic radiation HF-EMF are increasingly presentin the environment [1] because of the active developmentof wireless technology including cell phones Wi-Fi andvarious kinds of connected devices Since living material isnot a perfect dielectric it readily interferes with HF-EMFin a way that depends upon several parameters including(but not restricted to) its general shape the conductivityand density of the tissue and the frequency and amplitudeof the EMF The interaction between the living material

and the electromagnetic radiation may (or not) induce anelevation of the tissue temperature thus defining the thermal(versus nonthermal) associated metabolic responses In thecase of a thermal response the resulting heat dissipation isnormalized with the specific absorption rate (SAR) indexThis has led to considerable research efforts to study thepossible biological effects due to exposure to HF-EMFWhilethe vast majority of these studies have focused on animalsand humans because of health concerns with contradictoryor nonconclusive results [2] numerous experiments have alsobeen performed on plants Plants are outstanding modelscompared to animals to conduct such investigations theyare immobile and therefore keep a constant orientation inthe EMF and their specific scheme of development (highsurface area to volume ratio) makes them ideally suited toefficiently intercept EMF [3] It is also quite easy in plants to

Hindawi Publishing CorporationBioMed Research InternationalVolume 2016 Article ID 1830262 13 pageshttpdxdoiorg10115520161830262

2 BioMed Research International

120582

rarr

E

rarr

BDOP

(a) (b)

(c)

Rotating stirrer

Emitting antenna

Specialized plantculture chamber

(d)

Figure 1 Electromagnetic wave and experimental set-up (a) Schematic representation of an electromagnetic plane wave showing thetransverse and space varying electric (119864) and magnetic field (119861) The wavelength (120582) is the distance between two crests DOP directionof propagation (b) A TEM cell (transverse electromagnetic cell) (c) A GTEM cell (gigahertz transverse electromagnetic cell) (d) MSRC(mode stirred reverberation chamber) Note the double-sided metallic walls the emitting antenna the rotating stirrer and the specializedculture chamber that stands in the ldquoworking volumerdquo where the electromagnetic field characteristics have been extensively characterized

achieve genetically stable plant lines through the selection ofspecies that favor asexual reproduction [4] or self-pollination[5] Furthermore metabolic mutants are easily available forseveral species and constitute invaluable tools to understandthe way the EMF signal is transduced [6] Indeed severalreports have pointed out that plants actually perceive HF-EMF of even small amplitudes and transduce them intomolecular responses andor alterations of their developmen-tal scheme [3ndash9] The way that HF-EMF interact with plantsremains essentially unanswered However since EMF evokea multitude of responses in plants they might be consideredas a genuine environmental stimulus Indeed EMF exposurealters the activity of several enzymes including those ofreactive oxygen species (ROS) metabolism [7] a well-knownmarker of plant responses to various kinds of environmentalfactors EMF exposure also evokes the expression of specificgenes previously implicated in plant responses to wounding[5 8] and modifies the development of plants [9] Fur-thermore these responses are systemic insofar as exposureof only a small region of a plant results in almost imme-diate molecular responses throughout the plant [6] Theseresponses were abolished in the presence of calcium chelators[6] or inhibitors of oxidative phosphorylation [10] whichimplies the involvement of ATP pools In the present reviewwe describe exposure devices SAR determination methodsand biological responses (at both the cellularmolecular andwhole plant levels) observed after plant exposure to EMFWefocused this review on radiated (ie EMF that are emitted

through an antenna) HF-EMF (mainly within the rangeof 300MHzndash3GHz) and consequently will not address thebiological effects of static magnetic fields (SMF) extremelylow frequency electromagnetic fields (ELF) or HF currentinjection since their inherent physical properties are dramat-ically different from those of high frequencies Therefore theHF-EMF we consider should be viewed through the prismof classical electromagnetism macroscopic electrodynamicsphenomena described in terms of vector and scalar fields

2 Exposure Systems and Dosimetry

HF-EMF are a combination of an electric field and amagneticfield governed by Maxwellrsquos equations At high frequencythese vector quantities are coupled and obey wave equationswhether for propagating waves or for standing waves Invacuum the former travel at the speed of light (asymp3sdot108msminus1)and have the structure of a plane wave (Figure 1(a)) In othermedia the speed decreases and the spatial distribution for theelectric and the magnetic fields are generally arbitrary (thusnot being a plane wave) The latter which do not propagatebut vibrate up and down in place appear in some particularconditions (eg bounded medium like metallic cavity) andplay important roles inmany physical applications (resonatorwaveguide etc)

In both cases HF-EMF are characterized by an amplitudeof the electric (119864) or magnetic (119867) components (measuredin volts or amperes per meter) a frequency 119891 (number of

BioMed Research International 3

cycles per second of the wave quantity measured in hertz)and a wavelength 120582 (distance between wave crests measuredinmeters)These properties are related through the followingequation

120582 =

119888

119891

= 119888 times 119879 (1)

where 119888 is the speed of the wave in the considered mediumand119879 is the period of thewave (time between successive wavecrests measured in seconds) The wavelength 120582 is then thedistance traveled by the wave during a period 119879

The electromagnetic power density associated with anelectromagnetic wave (measured in watts per square meter)is obtained by a vector product between the electric andmagnetic field vectors (namely the Poynting vector) forevery point in space The total HF-EMF power crossingany given surface is derived from Poyntingrsquos theorem [11]For an incident plane wave in vacuum the time-averagedelectromagnetic power 119875

119894(measured in watts) illuminating a

surface of 1m2 orthogonal to the direction of propagation isgiven by the following equation

119875119894=

1198642

2 times 1198850

(2)

where 1198850is the characteristic impedance of free vacuum

space (377Ω)The absorbed electromagnetic power (119875119889) converted to

heat by Joule effect in a volume (119881) and averaged over a timeperiod is given by (3) for an electrically and magneticallylinear material that obeys Ohmrsquos law (conductivity 120590 insiemens per meter)

119875119889 =∭

V

120590 times 1198642

2

119889119881 (3)

21 Diversity of Exposure Devices Due to the wide varietyof electromagnetic waves physicians developed a lot of elec-tromagnetic exposure facilities mainly for electromagneticcompatibility (EMC) test purposes Some of these devices areused for plant exposure to HF-EMF

HF-EMF exposure set-up is usually made up with thefollowing two basic elements (i) HF source (radio frequencygenerator Gunn oscillator) associated with a radiating ele-ment (antenna strip-line) and (ii) a structure that allows thepropagation of EM waves and the exposure of the sampleThe simplest exposure set-up relies on the use of standardcell phones as a source of HF-EMF [12 13] radiating in anopen-area test site While this apparatus has the advantage ofbeing simple and economical it poses many limitations thatmay compromise the quality of the exposure Indeed thesecommunication devices are operated with different protocolsthat may modify or even interrupt the emitted powerAlso the biological samples are placed in the immediateneighborhood of the antenna which is a region where theelectromagnetic field is not completely established (near-field conditions) and therefore is difficult to measure thissituation may constitute an issue for bioelectromagnetics

studies These apparatuses are nowadays used only in a smallproportion of studies Moreover the use of open-area testsites exposes the biological samples to the uncontrolled elec-tromagnetic ambient environmentTheuse of shielded roomsis a good solution to overcome this issue Indeed anechoicchambers provide shielded enclosures which are designed tocompletely absorb reflected electromagnetic waves Howeverthese facilities are often large structures requiring specificequipment and costly absorbers to generate an incident planewave (far-field illumination) and are consequently seldomused for plant exposure [14 15]

In contrast numerous studies are based upon dedicatedapparatus of relatively small volume (Figure 1(b)) namelythe transverse electromagnetic (TEM) cell [16] TEM cellsare usually quite small (about 50 cm long times 20 cm wide)and therefore only allow the use of seeds or seedlings asplant models Many TEM cells are based upon the classicldquoCrawford cellrdquo [17] They consist of a section of rectangularcoaxial transmission line tapered at each end to adapt tostandard coaxial connectors A uniform plane wave of fixedpolarization and direction is generated in the sample spacefor experiments between the inner conductor (septum) andthe upper metallic wall Because this cost-efficient deviceis enclosed high amplitude EMF can be developed withrelatively little injected power Under some conditions twoparallel walls of the TEM cell can be removed (thereforeconstituting the so-called open TEM cell) without dramat-ically compromising the performances This configurationis adequate to allow plant lighting Special attention muststill be paid to the relative position of the samples in thesystem since the disposition of the different organs within theEMF could severely affect the efficiency of the plant samplesrsquocoupling with the electromagnetic field The main TEM celllimitation is that the upper useful frequency is bound by itsphysical dimensions limiting the practical size of samples athigh frequency

The gigahertz transverse electromagnetic (GTEM) cellhas emerged as a more recent EMF emission test facility(Figure 1(c)) [18] It is a hybrid between an anechoic chamberand a TEM cell and could therefore be considered as a highfrequency version of the TEM cellThe GTEM cell comprisesonly a tapered section with one port and a broadbandtermination This termination consists of a 50Ω resistorboard for low frequencies and pyramidal absorbers for highfrequenciesThis exposure device removes the inherent upperfrequency limit of TEM cell while retaining some of itsadvantages (mainly the fact that no antenna set-up is requiredand the fact that high field strength could be achieved withlow injected power)

Waveguides are another kind of screened enclosuresthat are seldom used in plant exposure [19 20] Theseclassical and easy to use exposure devices generate travelingwaves along the transmission coordinate and standing wavesalong the transverse coordinates In contrast to the TEMcell waveguides do not generate uniform plane waves butrather allow the propagation of more complex EMF namelypropagation modes Each mode is characterized by a cutofffrequency below which the mode cannot propagate Whenthe ends of the waveguide are short-circuited a so-called


resonant cavity is constituted fromwhich a recent large facil-ity originally designed for EMC studies namely the modestirred reverberation chamber (MSRC Figure 1(d)) is basedWhile this equipment is expensive and technically difficult toset up it is the state of the art in terms of electromagnetic fieldcharacteristics allowing the establishment of an isotropicand homogeneous field in a volume large enough to holda dedicated plant culture chamber (either transparent orshielded toward EMF [6]) This latter characteristic permitsexperiments on large plants that are kept in an adequatecontrolled environment [6] Our group pioneered the useof this facility based on judicious combinations of standingwaves patterns in a complex screened enclosure in plantbioelectromagnetics studies [8] and extensively described theMSRC functionality [21] Finally each exposure set-up maydiffer in concept polarization frequency or incident powerbut these setups always need to be optimally designed andbased onwell-understood physical concepts in order to assesswell-controlled HF-EMF exposure conditions (homogeneityrepeatability reproducibility etc)

22 Different Types of Exposure Signals From each of theprevious exposure devices two very different types of EMFcan be used to expose plants The most commonly encoun-tered mode is the continuous wave (CW) mode in whichthe biological samples are continuously exposed for a specificduration to an EMF of given frequency and amplitude (rarelymore than a fewdozenVmminus1)The secondmode is the pulsedelectromagnetic field (PEMF) mode in which the biologicalsamples are subjected to several series of discontinuous pulsesof ultrashort duration EMF (within the range of 120583s to ns)and usually of very high amplitude (up to several hundredkVmminus1) This last kind of exposure [22 23] is seldom usedbecause of the scarcity and great complexity of the equipmentneeded to generate the EMF and the difficulty to designthe dedicated antennae able to deliver such ultrashort powersurges [24]

The HF-EMF could also be modulated (ie varied intime at a given usually much lower frequency) Only a fewstudies explicitly addressed modulation effect on biologicalresponses Racuciu et al [25] exposedmaize caryopses to lowlevels (7 dBm) 900MHz RF field for 24 h in either contin-uous wave (CW) amplitude modulated (AM) or frequencymodulated (FM) modes They found that 12-day-old plantlengths were reduced by about 25 in modulated EMF (AMor FM type) compared to control (unexposed samples) whileCW exposure had an opposite (growth stimulation) effectsuggesting that EMFmodulation actually modifies biologicalresponses

23 Dosimetry In order to compare the biological effectsobserved in different exposure conditions the NationalCouncil on Radiation Protection andMeasurements officiallyintroduced in 1981 an EMF exposure metric the specificabsorption rate (SAR) The formal definition of this basicdosimetry (the amount of dose absorbed) is ldquothe time deriva-tive of the incremental energy absorbed (119889119882) by (dissipatedin) an incremental mass contained in a volume (119889119881) of

a given density 120588rdquo From this definition and (3) the SAR(measured in Wkgminus1) is given by the following equation

SAR = 119889119889119905

(

119889119882

120588 times 119889119881

) =

120590 times 1198642

2 times 120588

(4)

SAR is the power absorbed by living tissue during exposureto CW-EMF (this quantity does not apply to PEMF modebecause of the very short duration of the pulses that donot cause temperature increase in the samples) SAR can becalculated from the dielectric characteristics of plant tissuesat the working frequencies using (4) While 120588 could be easilydetermined the value of 120590 is dependent upon the frequencyand is difficult to assess in the range of GHz It is usuallyevaluated from the literature [40] since the experimentalset-up to measure this parameter at a given frequency(waveguide open waveguide and coaxial line technique egD-Line) is rarely used because of its complex set-up Fromthe biological heat-transfer equation the SAR can also bedetermined using the temperature increase evoked in planttissue after exposure to EMF using the following equation

SAR = 119862 times (119889119879119889119905

)

119905rarr0

(5)

where119862 is the heat capacity (J Kminus1 kgminus1 which is available forsome tissues in the literature) and 119889119879 (measured in Kelvin)is the sample temperature increase corresponding to theelapsed time 119889119905 (measured in second) since the beginningof HF-EMF exposure Either for animals or plants theSAR measurement is subject to uncertainty [46] Since thespecific heat is frequency independent and the temperaturedistribution is usuallymore uniform than the internal electricfield (5) provides for detectable temperature increases abetter way for SAR estimation

In animal and human tissue SAR is determined usingdedicated phantoms [47] filledwith a special liquid thatmim-ics the dielectric properties of biological fluids While thisapproach is adequate in animals in which the developmentalscheme produced volumes it could not be adapted to mostplant organs (eg leaves) that have a high surface area tovolume ratio [3] but could be used in fruits and tuberousstructures In contrast surface temperature can be easilyassessed with dedicated instruments (eg Luxtronreg fiberoptic temperature probe) and used to feed (5) [45] The SARcan also be determined using the differential power methodbased on the measurement of power absorption (reviewed in[48]) that takes place in the absence or presence of biologicalsamples [39] The SAR is then calculated by dividing theabsorbed power by the mass of the living material

3 Biological Responses

Biological responses should be considered as reporters ofand evidence for the plantrsquos ability to perceive and interactwith EMF These responses can take place at the subcellularlevel implyingmolecular events ormodification of enzymaticactivities or at the level of the whole plant taking the formof growth modification Tables 1ndash3 summarize some work


Table 1 Metabolic pathways affected after plant exposure to HF-EMF radiations

Enzymes or metabolites Metabolic pathways Organisms Exposure conditions Response to EMF

Phenylalanine ammonia-lyase Phenylpropanoids Phaseolus vulgaris NA (PEMF) Synergistic action with growthregulators in cultured cells [26]

Polyphenol oxidase Polyphenols Vigna radiata 900MHz up to 4 h855 120583Wcmminus2 85-fold increase [27]

120572- and 120573-amylases Starch metabolism Vigna radiata 900MHz up to 4 h855 120583Wcmminus2

25- and 15-fold increase for 120572-and 120573-amylases respectively [27]

120572- and 120573-amylases starchphosphorylases Starch metabolism Zea mays 1800MHz up to 4 h

332mWmminus22-fold increase for amylasesminus73 for starch phosphorylases

[28]

Water soluble sugars Sugar metabolism Phaseolus vulgaris 900MHz 4 h 2-fold reduction in soluble sugars[12]

Acid and alkaline invertases Sucrose metabolism Zea mays 1800MHz up to 4 h332mWmminus2

18- and 26-fold increase for acidand alkaline forms respectively

[28]Malate and NADP isocitratedehydrogenases glucose-6Pdehydrogenase

Krebs cycle pentosephosphate pathway Plectranthus 900MHz 1 h

Lower activity (minus10 to minus30) atthe end of the stimulus and thena 2-fold increase 24 h later [29]

ATP content and adenylateenergy charge (AEC) Energetic metabolism Solanum

lycopersicon900MHz 10min

5 Vmminus1Drop of ATP content (30) andAEC (08 to 06) 30min after the

stimulus [10]MDA content H

2O2

superoxide dismutasecatalase guaiacol peroxidaseglutathione reductaseascorbate peroxidase

Lipidperoxidation-oxidative

metabolismVigna radiata 900MHz 855 120583Wcmminus2

All oxidative metabolismmarkers increased (2-fold to

5-fold) [7]

MDA and H2O2content

catalase ascorbate peroxidase Lipid peroxidation Lemna minor 400 and 900MHz 2 to4 h 10 to 120Vmminus1

MDA and H2O2content catalase

and ascorbate peroxidaseactivities increased (10ndash30) [30]

Peroxidases Oxidative metabolism Vigna radiataLemna minor

900MHz 1 to 4 h855 120583Wcmminus2 or

41 Vmminus1Peroxidase activities increased

[18 27]

MDA oxidized and reducedglutathione NO synthase

Oxidativemetabolism-NOmetabolism

Triticum aestivum

245GHz 5 to 25 s126mWmmminus2

concomitantly withNaCl treatment

Exposure to EMF reduced theoxidative response of plants to

high salt treatment [31]

Protein metabolism-DNAdamage

Oxidative protein andDNA damage (comet

assay)Nicotiana tabacum 900MHz 23Vmminus1

Carbonyl content and tail DNAvalue increased (18-fold and

30 resp) [30]

Protein metabolism Protein contentPhaseolus vulgarisVigna radiata

Triticum aestivumCell phone 4 h

Drop in protein content inPhaseolus (71) and Vigna (57)

[27 32] and Triticum [13]

Amino acid metabolism Proline accumulation Zea mays Vignaradiata

940MHz 2 daysCell phone 2 h855 120583Wcmminus2

18- and 5-fold increase in Zmays [33] and V radiata [7]

respectively

Global terpene emission Monoterpenemetabolism

Petroselinumcrispum ApiumgraveolensAnethumgraveolens

900ndash2400MHz70ndash100mWmminus2

Enhanced emission of terpenecompounds [34]

reporting HF-EMF effects observed at the scale of the wholeplant biochemical processes or gene regulation respectively

31 Cellular andMolecular Level Numerous reports [4 7 33]indicate an increase in the production of malondialdehyde

(MDA a well-known marker of membrane alteration) alongwith ROSmetabolism activation after exposing plants to HF-EMF (Table 1) Membrane alteration and ROS metabolismactivation are likely to establish transduction cascades thatenable specific responses Indeed the critical role of calcium


Table 2 Genes whose expression is altered after plant exposure to HF-EMF

Gene Organism Function Exposure conditions Response to EMFexposure

lebZIP1 Solanum lycopersicon whole plant Transcription factor 900MHz 5Vmminus1 CWin a MSRC

Increase (3-fold to4-fold) [6 8]

lebZIP1 Solanum lycopersicon whole plant Transcription factor Cell phone Increase (3-4-fold)[35]

cam Solanum lycopersicon whole plant Ca2+ signal transduction 900MHz 5Vmminus1 CWin a MSRC

Increase (5-fold)[5 10]

cdpk Solanum lycopersicon whole plant Ca2+ signal transduction 900MHz 5Vmminus1 CWin a MSRC Increase (5-fold) [10]

cmbp Solanum lycopersicon whole plant mRNAmetabolism 900MHz 5Vmminus1 CWin a MSRC Increase (6-fold) [5]

pin2 Solanum lycopersicon whole plant Proteinase inhibitor 900MHz 5Vmminus1 CWin a MSRC

Increase (45-fold [5]and 25-fold) [6]

pin2 Solanum lycopersicon whole plant Proteinase inhibitor 900MHz cell phone Increase (2-fold) [35]

At4g26260 Arabidopsis thaliana cell suspensionculture

Similar to myo-inositoloxygenase 19 GHz 8mWcmminus2 Decrease (03-fold)

[36]


Glutamine-dependentasparagine synthetase 19 GHz 8mWcmminus2 Decrease (04-fold)

[36]

At3g15460 Arabidopsis thaliana cell suspensionculture Brix domain protein 19 GHz 8mWcmminus2 Decrease (05-fold)

[36]

At4g39675 Arabidopsis thaliana cell suspensionculture Expressed protein 19 GHz 8mWcmminus2 Increase (15-fold)

[36]


[36]

AtCg00120 Arabidopsis thaliana cell suspensionculture

ATPase alpha subunit(chloroplast) 19 GHz 8mWcmminus2 Increase (14-fold)

[36]

a crucial second messenger in plants has long been pointedout [6 10] the responses (eg changes in calm-n6 lecdpk-1 and pin2 gene expression) to EMF exposure are severelyreduced when plants are cultivated with excess of calcium orin the presence of calcium counteracting agents (Figure 2)such as chelators (EGTA and BAPTA) or a channel blocker(LaCl

3) The importance of calcium in the establishment of

the plant response is also highlighted by the fact that earlygene expression associated with EMF exposure involves atleast 2 calcium-related products (calmodulin and calcium-dependent protein kinase) [5 10] This response is alsoenergy-dependent an important drop (30 Figure 3) inATPcontent and adenylate energy charge (AEC) occurs after HF-EMF exposure [10] It is not clear for now if the AEC dropis the consequence of altered membranes allowing passiveATP exit or if higher consumption of ATP occurred becauseof increased metabolic activity Indeed it is well known thata drop in AEC stimulates the catabolic enzymatic pathwaysthrough allostericmodulations Nevertheless inhibiting ATPbiosynthesis with the decoupling agent carbonyl cyanide m-chlorophenyl hydrazone (CCCP) abolished plant responsesto EMF exposure [10] Nitric oxide (NO) is another signalingmolecule that is tightly related to environmental factorsrsquoimpact on plants [49] NO rapidly increases after variouskinds of stimuli including drought stress or wounding Chenet al [50] recently demonstrated the increased activity ofnitric oxide synthase and accumulation of NO after exposing

caryopses of wheat for 10 s to high power 245GHz EMFSimilarly Qiu et al [51] showed in wheat that the toler-ance to cadmium evoked by microwave pretreatment wasabolished by the addition of 2-(4-carboxyphenyl)-4455-tetramethylimidazoline-1-oxyl-3-oxide (carboxy-PTIO) anNO scavenger suggesting that microwave-induced NO pro-duction was involved in this mechanism Taken togetherthese results advocate for the EMF induction of NO synthaseHowever these studies used high power EMF (modifiedmicrowave oven) as stimulating tool and the fact that a tem-perature increase of the sample was the cause of NO increaseis not excluded To our knowledge the involvement of NOhas not yet been demonstrated after low power (ie non-thermal) EMF exposure Furthermore well-known actors ofplant responses to environmental stimuli are also involvedthe tomato mutants sitiens and JL-5 for abscisic (ABA) orjasmonic (JA) acids biosynthesis respectively display normalresponses (accumulation of stress-related transcripts) whenwhole plants are exposed to EMF [6] In contrast veryrapid distant responses to local exposure that occur in thewild plants (Figure 4(a)) are impaired in sitiens ABA mutant(Figure 4(b)) and JL-5mutants highlighting the existence ofa transmitted signal (whose genesis andor transmission isdependent on ABA and JA) in the whole plant after localexposure [6] The nature of this signal is still unknown butvery recent work has demonstrated that membrane potentialis affected after exposure to EMF [14] It could therefore be


Table 3 Morphogenetic responses observed after plant exposure to HF-EMF

Plant species Exposure conditions Responses to HF-EMF exposure and references

Raphanus sativus Gunn generator 105 GHz 14mW exposureof seeds and hypocotyls

Germination inhibition (45) reduction ofhypocotyl elongation (40) [37]

Lens culinaris Cell phone 1800MHz (1mW) exposure ofdormant seeds

Reduction of seedlingsrsquo root growth (60) andmitotic index (12) Abnormal mitosis increased

(52) [38]

Vigna radiata Cell phone 900MHz 855 120583Wcmminus2 Rhizogenesis (root number and length) severelyaffected [7]

Vigna radiata Cell phone 900MHz 855 120583Wcmminus2Inhibition of germination (50) hypocotyl(46) and root growth (59) Dry weight

reduced by 43 [27]

Phaseolus aureus Vigna radiata Cell phone 4 h exposure Root and stem elongations severely affected (minus44and minus39 resp) [12 32]

Vigna radiata Lablab purpureus 18 GHz 048ndash145mWcmminus2 Reduction of height and fresh weight [39]

Zea mays 1 GHz 1 to 8 h 047Wcmminus2 Reduced growth of 12-day-old plants (about 50after 8 h of exposure) [40]

Zea mays 1800MHz 4 h 332mWmminus2 Reduced growth of roots and coleoptiles (16 and22 resp) [28]

Vigna radiata Triticum aestivum Cell phone 900MHz 4 h exposure Growth reduction (21 and 50) in Vigna andTriticum respectively [13]

Triticum aestivum Cicer arietinumVigna radiata Vigna aconitifolia

Klystron-based EMF generator 96GHz1 dBm to 35 dBm Growth and biomass reduction [41]

Vigna radiata Ipomoea aquatica 425MHz 2 h 1mW Growth stimulation of primary root [16]

Glycine max 900MHz 57 to 41 Vmminus1 Inhibition of epicotyl andor root growthdepending on exposure set-up [9]

Lemna minor 400ndash1900MHz 23 to 390Vmminus1 wholeplant exposure

Growth slowed down at least in the first daysfollowing exposure [18]

Trigonella foenum-graecum Pisumsativum 900MHz 05ndash8 h Increased root size nodule number and size [42]

Hibiscus sabdariffa Resulting field from a GSM base antenna(not measured)

Reduction of flower bud abscission withincreasing distances from the antenna [43]

Linum usitatissimum Cell phone or Gunn generator (105GHz) 2 h Production of epidermic meristems undercalcium deprivation condition [44]

Rosa hybrida 900MHz 5ndash200Vmminus1 whole plantexposure in MSRC

Delayed and reduced (45) growth of secondaryaxes [45]

hypothesized that electrical signals (action potential andorvariation potential) could be the transmitted signal stronglyimplying that HF-EMF is a genuine environmental factor

311 Alterations of Enzymatic Activities Table 1 summarizessome of the enzymatic activities that aremodified after expos-ing plants to HF-EMF As previously noted ROS metabolismis very often activated after plant exposure to EMF Enzymaticactivities such as peroxidase catalase superoxide dismutaseand ascorbate peroxidase have twofold to fourfold increase[4 7 18 27 33] The question remains open to determine ifthis could be the consequence of a direct action of EMF onliving tissue Indeed the very low energy that is associatedwith the EMF at these frequencies makes them nonionizingradiations Side effects of elevated ROS metabolism are alsonoted H

2O2production [4 7] MDA increases [4 7 33] and

protein damage [30] An increase in polyphenol oxidase [27]and phenylalanine ammonia-lyase [26] may indicate stress

responses linked to an increased lignification a commonresponse of plants to environmental stress

Protein content is reduced in Vigna and Phaseolus [2732] as well as in Triticum [13] It is not yet known if thedecrease in protein content results froman increase in proteindegradation andor a decrease in protein synthesis but thismay constitute a stimulating field of investigation sinceevidence shows that mRNA selection from translation occursafter plant exposure to HF-EMF [10] Hydrolytic enzymaticactivities (120572- and 120573-amylases and invertases) responsiblefor the production of soluble sugar increase in germinatingseeds after exposure to HF-EMF [12 28 32] while thestarch phosphorylase activity phosphorolytic and potentiallyreversible is diminished In contrast HF-EMF exposurecauses a drop of soluble sugar that may be related to theinhibition of Krebs cycle and pentose phosphate pathway inPlectranthus (Lamiaceae) leaves after exposure to 900MHzEMF [29] suggesting that seeds and adult leaves respond in


0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast

(a) Standard (073mM calcium)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast

(b) Standard + calcium (73mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast

(c) Standard minus calcium (0M)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)

Figure 2 Effect of calcium concentration in culture medium on calm-n6 (calmodulin) pin2 (proteinase inhibitor) and lecdpk1 (calcium-dependent protein kinase) transcript accumulation in response to the HF-EMF exposure (a) Standard medium (073mM of calcium)(b) Tenfold extra calcium (73mM) (c) No calcium (0mM) (d) No calcium (0mM) with 05mM of EGTA (e) No calcium (0mM) with04mMof BAPTA (12-bis(o-aminophenoxy)ethane-NNN1015840N1015840-tetraacetic acid) a specificCa2+ chelator (f) No calcium (0mM)with 01mMLaCl3 Bars representmean values plusmn SE from at least three independent experiments An asterisk over the bars states the significant differences

according to the one-sided Mann-Whitney 119880 test Reproduced from [10] with permission


0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)

Figure 3 ATP concentration and adenylate energy charge (AEC) changes after HF-EMF exposure (5Vmminus1 10min) in a mode stirredreverberation chamber C control unexposed plants 15 30 and 60 time (min) after the end of HF-EMF exposure (a) ATP concentration(pmolmgminus1 Prot) (b) Adenylate energy charge (ratio) Bars represent mean values plusmn SE from at least three independent experimentsAn asterisk over the bars states the significant differences according to the one-sided Mann-Whitney 119880 test Reproduced from [10] withpermission

Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15

Terminal leafLeaf 1(b)

Figure 4 Local and systemic responses after HF-EMF exposure (a) Systemic response after local exposure to HF-EMF in wild type Localand distant responses after stimulation of leaf 1 (with the rest of the plant being protected from the EMF) The stimulated tissue (leaf 1) anddistant one (terminal leaf) both displayed responses (accumulation of pin2 transcript) HF-EMF exposure 5 Vmminus1 10min (b) Impairmentof distant response after exposure to HF-EMF in sitiens (ABA deficient) mutant The stimulated tissue (leaf 1) displays the response to EMFexposure (accumulation of pin2 transcript) while the response in the distant tissue (terminal leaf) is impaired HF-EMF exposure 5 Vmminus110min Reproduced from [6] with permission

a different way to HF-EMF exposure The accumulation ofproline reported by several authors [7 33] and an increasein terpenoid emission and content in aromatic plants [34] arealso classical responses of plants to environmental stresses

312 Modification of Gene Expression While numerousreports focused on enzymatic activities alterations afterexposure to EMF only a few studies concentrate on geneexpression modifications (Table 2) Tafforeau et al [44]demonstrated usingGunn generator (105GHz) several repro-ducible variations in 2D gel electrophoresis profiles showingthat gene expression is likely to be altered by the exposuretreatment Jangid et al [52] provided indirect proof (RAPDprofiles) suggesting that high power microwave irradiation(2450MHz 800Wcmminus2) modifies gene expression in Vigna

aconitifolia while these results do not exclude a possiblethermal effect of microwave treatment Arabidopsis thalianasuspension-cultured cells exposed to HF-EMF (19GHz8mWcmminus2) showed differential expression of several genes(119901 values lt 005) compared to the control (unexposed)condition in microarray analysis [36] Most of them aredownregulated (whileAt4g39675 At5g10040 andAtCg00120displayed a slight increase see Table 2) However the RT-PCR 119901 value lowers the significance of these variations andthese authors consequently concluded the absence of HF-EMF effect on plant gene expression In contrast short dura-tion high frequency low amplitude EMF exposure (10min900MHz 5Vmminus1) performed on whole 3-week-old toma-toes in MSRC [5 6 8 10] demonstrated altered expressionsof at least 5 stress-related genes (Table 2) suggesting that


whole plants are more sensitive to HF-EMF than culturedcells These experiments have been independently replicatedby Rammal et al [35] using a longer exposure period anda far less sophisticated exposure set-up (cell phone) Stressresponses of plants quite often display a biphasic pattern [53]a very rapid increase in transcript accumulation that lasts 15ndash30min followed by a brief return to basal level and thena second increase (after 60min) This pattern was observedafter tomato exposure to EMF so we questioned the meaningof the early and late population of transcripts in terms ofphysiological significance by measuring their association topolysomes (which reflects their putative translation to pro-teins) We found that the early (0ndash15min) mRNA populationwas only faintly associated with polysomes yet being poorlytranslatedwhile the latemRNApopulation (60min) is highlyassociated with polysomes [10] This result strongly suggeststhat only the late mRNA populationmay have a physiologicalimportance since it is the only one to be efficiently translatedinto proteins

32 Whole Plant Level The biochemical and molecularmodifications observed after plant exposure to EMF anddescribed in the previous paragraphs might induce mor-phogenetic alterations of plant development Indeed anincreasing number of studies report modifications of plantgrowth after exposure toHF-EMF (Table 3)These treatmentsare effective at different stages of plant development (seedsseedlings or whole plants) and may affect different organsor developmental processes including seeds germination andstem and root growth indicating that biological samples ofeven small sizes (a few mm) are able to perceive HF-EMFSeed exposure to EMF generally results in a reduced germi-nation rate [27 37 39] while in other cases germination isunaffected [42] or even stimulated [16] The seedlings issuedfrom EMF-exposed seeds displayed reduced growth of rootsandor stem [13 28 32 37ndash39 41] but rarely a stimulatoryeffect [16] This point strongly differs from exposure to staticmagnetic fields or extremely low frequency EMF inwhich thestimulatory effects on growth are largely predominant [54]Ultrashort pulsed high power EMF (PEMF 4120583s 93 GHz320 kVmminus1) also tends to stimulate germination of seedsof radish carrot and tomato and increase plant height andphotosynthetic surface area in radish and tomato [20] androots of tobacco seedlings [22] These different effects ofPEMF compared to HF-EMF on plants may be related totheir fundamental difference in terms of physical propertiesExposure to HF-EMF of seedlings or plants (rather thanseeds) also generally resulted in growth inhibition [9 18 2728 39] Singh et al [7] showed that rhizogenesis (root numberand length) is severely affected in mung bean after exposureto cell phone radiation possibly through the activation ofseveral stress-related enzymes (peroxidases and polyphenoloxidases) Akbal et al [38] showed that root growth wasreduced by almost 60 in Lens culinaris seeds exposed in thedormant state to 1800MHz EMF radiation Concomitantlythese authors reported an increase in ROS-related enzymeslipid peroxidation and proline accumulation with all ofthese responses being characteristic of plant responses to

stressful conditions Afzal and Mansoor [13] investigatedthe effect of a 72 h cell phone exposure (900MHz) onboth monocotyledonous (wheat) and dicotyledonous (mungbean) plants seeds germination was not affected while theseedlings of both species displayed growth inhibition proteincontent reduction and strong increase in the enzymaticactivities of ROS metabolism It is however worth notingthat growth of mung bean and water convolvulus seedlingsexposed at a lower frequency (425MHz 2 h 1mW) isstimulated because of higher elongation of primary root[11] while duckweed (Lemna minor Araceae) growth wassignificantly slowed down not only by exposure at a similarfrequency (400MHz 4 h 23Vmminus1) but also after exposure at900 and 1900MHz for different field amplitudes (23 41 and390Vmminus1) at least in the first days following the exposure[18] Surducan et al [15] also found stimulation of seedlinggrowth in bean andmaize after exposure to EMF (2452GHz0005mWcmminus2) Senavirathna et al [55] studied real-timeimpact of EMF radiation (2GHz 142Wmminus2) on instanta-neous growth in the aquatic plant parrotrsquos feather (Myrio-phyllum aquaticum Haloragaceae) using nanometer scaleelongation rate fluctuationsThese authors demonstrated thatEMF-exposed plants displayed reduced fluctuation rates thatlasted for several hours after the exposure strongly suggestingthat plantsrsquo metabolism experienced a stressful situation Itis worth noting that the exposure did not cause any plantheating (as measured using sensitive thermal imaging) Someother kind ofmorphological changes also occurred after plantexposure to HF-EMF induction of epidermal meristems inflax [44] flower bud abscission [43] nitrogen-fixation nodulenumber increase in leguminous [42] or delayed reducedgrowth of secondary axis in Rosa [45]

These growth reductions may be related to a lowerphotosynthetic potential since Racuciu et al [40] showed thatexposing 12-day-old maize seedlings to 047Wkgminus1 1 GHzEMF induces a drop in photosynthetic pigment content thediminution was especially important in chlorophyll a whichwas reduced by 80 after 7 h of exposure Ursache et al[56] showed that exposure of maize seedlings to microwave(1mWcmminus2 1075GHz) also caused a drop in chlorophylla and b content Similarly Hamada [57] found a decrease inchlorophyll content in 14-day-old seedlings after exposingthe caryopses for 75min at 105 GHz Kumar et al showed a13 decrease in total chlorophyll after 4 h exposure of maizeseedlings to 1800MHz (332mWmminus2) These modificationsmay be related to abnormal photosynthetic activity whichrelies on many parameters including chlorophyll andcarotenoid content Senavirathna et al [58] showed thatexposing duckweeds to 2ndash8GHz 45ndash50Vmminus1 EMF inducedchanges in the nonphotosynthetic quenching indicatinga potential stressful condition Three aromatic speciesbelonging to Apiaceae family (Petroselinum crispum Apiumgraveolens and Anethum graveolens) strongly respond toglobal system for mobile communications radiation (GSM09GHz 100mWcmminus2) or wireless local area network(WLAN 245GHz 70mWcmminus2) exposure by decreasingthe net assimilation rate (over 50) and the stomatalconductance (20ndash30) [34]


4 Conclusion and Future Prospects

An increasing number of reports highlight biologicalresponses of plants after exposure to HF-EMF at themolecular and the whole plant levelThe exposure conditionsare however far from being standardized and illustrate thediversity of exposure conditions employed However futurework should avoid exposure in near-field conditions (ie inimmediate vicinity of the emission antenna) where the fieldis instable and difficult to characterize Similarly the use ofcommunication devices (ie cell phones) should be avoidedas emission sources since it may be difficult to readily controlthe exposure conditions because of built-in automationthat may overcome the experimental set-up The use ofspecialized devices (TEM cells GTEM cell waveguidesMSRC etc) in which a precise control of exposure conditioncan be achieved is highly preferable

Shckorbatov [59] recently reviewed the possible interac-tions mechanisms of EMF with living organisms While theclassical targets (interaction with membranes free radicalsand intracellular regulatory systems) have all been observedin plants a convincing interpretation of the precise mech-anism of HF-EMF interaction with living material is stillneeded Alternative explanation (ie electromagnetic reso-nance achieved after extremely high frequency stimulationwhich matches some kind of organ architecture) has alsobeen proposed for very high frequency EMF (several dozenGHz) [60] However the reality of this phenomenon in vivo(studied for now only through numerical simulations) and itsformal contribution to the regulation of plant developmenthave not yet been experimentally established Amat et al[61] proposed that light effects on plants arose not onlythrough chromophores but also through alternating electricfields which are induced in the medium and able to interactwith polar structures through dipole transitionsThe possibleassociated targets (ATPADP ratio ATP synthesis and Ca2+regulation) are also those affected by exposure to HF-EMF[10] It could therefore be speculated that HF-EMF mayuse similar mechanisms The targeted pathways especiallyCa2+ metabolism are well known to modulate numerousresponses of plants to environmental stress While deeperunderstanding of plant responses to HF-EMF is still neededthese treatments may initiate a set of molecular responsesthat may affect plant resistance to environmental stresses asalready demonstrated in wheat for CaCl

2[62] or UV [63]

tolerances and constitute a valuable strategy to increase plantresistance to environmental stressful conditions

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors would like to gratefully acknowledge the LRCBIOEM (ldquoLaboratoire de Recherche ConventionnerdquomdashLRCno 002-2011-CEA DAMInstitut Pascal) for its financialsupport

References

[1] A Balmori ldquoElectromagnetic pollution from phone mastsEffects on wildliferdquo Pathophysiology vol 16 no 2-3 pp 191ndash1992009

[2] HKleinlogel TDierks TKoenigH LehmannAMinder andR Berz ldquoEffects of weak mobile phonemdashelectromagnetic fields(GSM UMTS) on well-being and resting EEGrdquo Bioelectromag-netics vol 29 no 6 pp 479ndash487 2008

[3] A Vian C Faure S Girard et al ldquoPlants respond to GSM-likeradiationsrdquo Plant Signaling amp Behavior vol 2 no 6 pp 522ndash524 2007

[4] M Tkalec K Malaric and B Pevalek-Kozlina ldquoExposure toradiofrequency radiation induces oxidative stress in duckweedLemna minor Lrdquo Science of the Total Environment vol 388 no1ndash3 pp 78ndash89 2007

[5] D Roux A Vian S Girard et al ldquoElectromagnetic fields(900MHz) evoke consistent molecular responses in tomatoplantsrdquo Physiologia Plantarum vol 128 no 2 pp 283ndash2882006

[6] E Beaubois S Girard S Lallechere et al ldquoIntercellular com-munication in plants evidence for two rapidly transmittedsystemic signals generated in response to electromagnetic fieldstimulation in tomatordquo Plant Cell and Environment vol 30 no7 pp 834ndash844 2007

[7] H P Singh V P Sharma D R Batish and R K KohlildquoCell phone electromagnetic field radiations affect rhizogenesisthrough impairment of biochemical processesrdquo EnvironmentalMonitoring and Assessment vol 184 no 4 pp 1813ndash1821 2012

[8] A Vian D Roux S Girard et al ldquoMicrowave irradiation affectsgene expression in plantsrdquo Plant Signaling and Behavior vol 1no 2 pp 67ndash69 2006

[9] M N Halgamuge S K Yak and J L Eberhardt ldquoReducedgrowth of soybean seedlings after exposure to weak microwaveradiation from GSM 900 mobile phone and base stationrdquoBioelectromagnetics vol 36 no 2 pp 87ndash95 2015

[10] D Roux A Vian S Girard et al ldquoHigh frequency (900MHz)low amplitude (5V mminus1) electromagnetic field a genuineenvironmental stimulus that affects transcription translationcalcium and energy charge in tomatordquo Planta vol 227 no 4pp 883ndash891 2008

[11] J A Stratton ElectromagneticTheory McGraw-Hill New YorkNY USA 1941

[12] V P Sharma H P Singh R K Kohli and D R BatishldquoMobile phone radiation inhibits Vigna radiata (mung bean)root growth by inducing oxidative stressrdquo Science of the TotalEnvironment vol 407 no 21 pp 5543ndash5547 2009

[13] M Afzal and S Mansoor ldquoEffect of mobile phone radiationson morphological and biochemical parameters of Mung bean(Vigna radiata) andwheat (Triticum aestivum) seedlingsrdquoAsianJournal of Agricultural Sciences vol 4 no 2 pp 149ndash152 2012

[14] M D H J Senavirathna and T Asaeda ldquoRadio-frequencyelectromagnetic radiation alters the electric potential ofMyrio-phyllum aquaticumrdquo Biologia Plantarum vol 58 no 2 pp 355ndash362 2014

[15] E Surducan V Surducan A Butiuc-Keul and A HalgamagyldquoMicrowaves irradiation experiments on biological samplesrdquoStudia Univesitas Babes-Bolyai Biologia vol 58 no 1 pp 83ndash982013

[16] P Jinapang P Prakob P Wongwattananard N E Islam and PKirawanich ldquoGrowth characteristics of mung beans and water


convolvuluses exposed to 425-MHz electromagnetic fieldsrdquoBioelectromagnetics vol 31 no 7 pp 519ndash527 2010

[17] M L Crawford ldquoGeneration of standard EM fields usingTEM transmission cellsrdquo IEEE Transactions on ElectromagneticCompatibility vol 16 no 4 pp 189ndash195 1974

[18] M Tkalec K Malaric and B Pevalek-Kozlina ldquoInfluence of400 900 and 1900MHz electromagnetic fields on Lemnaminorgrowth and peroxidase activityrdquoBioelectromagnetics vol 26 no3 pp 185ndash193 2005

[19] L M Liu F Garber and S F Cleary ldquoInvestigation of theeffects of continuous-wave pulse- and amplitude-modulatedmicrowaves on single excitable cells of chara corallinardquo Bioelec-tromagnetics vol 3 no 2 pp 203ndash212 1982

[20] A Radzevicius S Sakalauskiene M Dagys et al ldquoThe effect ofstrong microwave electric field radiation on (1) vegetable seedgermination and seedling growth raterdquo Zemdirbyste vol 100no 2 pp 179ndash184 2013

[21] S Lallechere S Girard D Roux P Bonnet F Paladian and AVian ldquoMode Stirred Reverberation Chamber (MSRC) a largeand efficient tool to lead high frequency bioelectromagnetic invitro experimentationrdquo Progress in Electromagnetics Research Bvol 26 pp 257ndash290 2010

[22] G Cogalniceanu M Radu D Fologea and A Brezeanu ldquoShorthigh-voltage pulses promote adventitious shoot differentiationfrom intact tobacco seedlingsrdquo Electro- and Magnetobiologyvol 19 no 2 pp 177ndash187 2000

[23] KDymek PDejmekV Panarese et al ldquoEffect of pulsed electricfield on the germination of barley seedsrdquo LWTmdashFood Scienceand Technology vol 47 no 1 pp 161ndash166 2012

[24] B Cadilhon L Pecastaing S Vauchamp J Andrieu VBertrand and M Lalande ldquoImprovement of an ultra-wide-band antenna for high-power transient applicationsrdquo IETMicrowaves Antennas and Propagation vol 3 no 7 pp 1102ndash1109 2009

[25] M Racuciu S Miclaus and D E Creanga ldquoNon-thermalcontinuous and modulated rf field effects on vegetal tissuedeveloped from exposed seedsrdquo in Electromagnetic Field Healthand Environment A Krawczyk R Kubacki S Wiak and CLemos Antunes Eds vol 29 of Studies in Applied Electromag-netics and Mechanics pp 142ndash148 IOS Press Amsterdam TheNetherlands 2008

[26] D B Jones G P Bolwell and G J Gilliatt ldquoAmplificationby pulsed electromagnetic fields of plant growth regulatorinduced phenylalanine ammonia-lyase during differentiation insuspension cultured plant cellsrdquo Electromagnetic Biology andMedicine vol 5 no 1 pp 1ndash12 1986

[27] V P Sharma H P Singh D R Batish and R K KohlildquoCell phone radiations affect early growth of vigna radiate(Mung Bean) through biochemical alterationsrdquo Zeitschrift furNaturforschung C vol 65 no 1-2 pp 66ndash72 2010

[28] A Kumar H P Singh D R Batish S Kaur and R K KohlildquoEMF radiations (1800MHz)-inhibited early seedling growthof maize (Zea mays) involves alterations in starch and sucrosemetabolismrdquo Protoplasma pp 1ndash7 2015

[29] M Kouzmanova M Dimitrova D Dragolova G AtanasovaandN Atanasov ldquoAlterations in enzyme activities in leaves afterexposure ofPlectranthus Spplants to 900MHZelectromagneticfieldrdquo Biotechnology amp Biotechnological Equipment vol 23supplement 1 pp 611ndash615 2009

[30] S Radic P Cvjetko K Malaric M Tkalec and B Pevalek-Kozlina ldquoRadio frequency electromagnetic field (900MHz)

induces oxidative damage to DNA and biomembrane intobacco shoot cells (Nicotiana tabacum)rdquo in Proceedings ofthe IEEEMTT-S International Microwave pp 2213ndash2216 IEEEHonolulu Hawaii USA June 2007

[31] Y-P Chen J-F Jia and Y-J Wang ldquoWeak microwave canenhance tolerance of wheat seedlings to salt stressrdquo Journal ofPlant Growth Regulation vol 28 no 4 pp 381ndash385 2009

[32] V P Sharma G Singh and R K Kohli ldquoEffect of mobilephone EMF on biochemical changes in emerging seedlings ofPhaseolus aureus RoxbrdquoThe Ecoscan vol 3 no 3-4 pp 211ndash2142009

[33] H Zare S Mohsenzadeh and A Moradshahi ldquoElectromag-netic waves from GSM a mobile phone simulator and abioticstress in Zea mays Lrdquo Journal of Nutrition amp Food Sciences volS11 p 3 2015

[34] M-L Soran M Stan U Niinemets and L Copolovici ldquoInflu-ence of microwave frequency electromagnetic radiation onterpene emission and content in aromatic plantsrdquo Journal ofPlant Physiology vol 171 no 15 pp 1436ndash1443 2014

[35] M Rammal F Jebai H Rammal and W H Joumaa ldquoEffectsof long term exposure to RFMW radiations on the expressionofmRNAof stress proteins in Lycopersicon esculentumrdquoWSEASTransactions on Biology and Biomedicine vol 11 pp 10ndash14 2014

[36] J C Engelmann R Deeken T Muller G Nimtz M R GRoelfsema and R Hedrich ldquoIs gene activity in plant cellsaffected by UMTS-irradiation A whole genome approachrdquoAdvances and Applications in Bioinformatics and Chemistry vol1 pp 71ndash83 2008

[37] A Scialabba and C Tamburello ldquoMicrowave effects on germi-nation and growth of radish (Raphanus sativus L) seedlingsrdquoActa Botanica Gallica vol 149 no 2 pp 113ndash123 2002

[38] A Akbal Y Kiran A Sahin D Turgut-Balik and H H BalikldquoEffects of electromagnetic waves emitted by mobile phones ongermination root growth and root tip cell mitotic division ofLens culinaris Medikrdquo Polish Journal of Environmental Studiesvol 21 no 1 pp 23ndash29 2012

[39] Y C Chen and C Chen ldquoEffects of mobile phone radiation ongermination and early growth of different bean speciesrdquo PolishJournal of Environmental Studies vol 23 no 6 pp 1949ndash19582014

[40] M Racuciu C Iftode and S Miclaus ldquoInhibitory effects of lowthermal radiofrequency radiation on physiological parametersof Zeamays seedlings growthrdquoRomanian Journal of Physics vol60 no 3-4 pp 603ndash612 2015

[41] L Ragha S Mishra V Ramachandran and M S BhatialdquoEffects of low-power microwave fields on seed germinationand growth raterdquo Journal of Electromagnetic Analysis andApplications vol 3 no 5 pp 165ndash171 2011

[42] S Sharma and L Parihar ldquoEffect of mobile phone radiationon nodule formation in the leguminous plantsrdquo Current WorldEnvironment Journal vol 9 no 1 pp 145ndash155 2014

[43] A O Oluwajobi O A Falusi and N A Zubbair ldquoFlowerbud abscission reduced in hibiscus sabdariffa by radiation fromGSMmastrdquo Environment and Pollution vol 4 no 1 2014

[44] M Tafforeau M-C Verdus V Norris et al ldquoPlant sensitivityto low intensity 105GHz electromagnetic radiationrdquo Bioelectro-magnetics vol 25 no 6 pp 403ndash407 2004

[45] A Gremiaux S Girard V Guerin et al ldquoLow-amplitude high-frequency electromagnetic field exposure causes delayed andreduced growth in Rosa hybridardquo Journal of Plant Physiologyvol 190 pp 44ndash53 2016


[46] V J Berdinas-Torres Exposurersquos systems and dosimetry of large-scale in vivo studies [PhD thesis] Swiss Federal Institute ofTechnology Zurich Switzerland 2007

[47] M J Van Wyk M Bingle and F U C Meyer ldquoAntenna mod-eling considerations for accurate SAR calculations in humanphantoms in close proximity to GSM cellular base stationantennasrdquo Bioelectromagnetics vol 26 no 6 pp 502ndash509 2005

[48] S Miclaus and M Racuciu ldquoA dosimetric study for experi-mental exposures of vegetal tissues to radiofrequency fieldsrdquo inElectromagnetic Field Health and Environment A KrawczykR Kubacki S Wiak and C Lemos Antunes Eds vol 29 ofStudies in Applied Electromagnetics and Mechanics pp 133ndash141IOS Press Amsterdam The Netherlands 2008

[49] J Leon M C Castillo A Coego J Lozano-Juste and RMir ldquoDiverse functional interactions between nitric oxide andabscisic acid in plant development and responses to stressrdquoJournal of Experimental Botany vol 65 no 4 pp 907ndash921 2014

[50] Y-P Chen J-F Jia and X-L Han ldquoWeak microwave canalleviate water deficit induced by osmotic stress in wheatseedlingsrdquo Planta vol 229 no 2 pp 291ndash298 2009

[51] Z-B Qiu J-L Guo M-M Zhang M-Y Lei and Z-L LildquoNitric oxide acts as a signal molecule in microwave pretreat-ment induced cadmium tolerance in wheat seedlingsrdquo ActaPhysiologiae Plantarum vol 35 no 1 pp 65ndash73 2013

[52] R K Jangid R Sharma Y Sudarsan S Eapen G Singhand A K Purohit ldquoMicrowave treatment induced mutationsand altered gene expression in Vigna aconitifoliardquo BiologiaPlantarum vol 54 no 4 pp 703ndash706 2010

[53] A Vian C Henry-Vian and E Davies ldquoRapid and systemicaccumulation of chloroplast mRNA-binding protein transcriptsafter flame stimulus in tomatordquo Plant Physiology vol 121 no 2pp 517ndash524 1999

[54] J A Teixeira da Silva and J Dobranszki ldquoMagnetic fields how isplant growth and development impactedrdquo Protoplasma 2015

[55] M D H J Senavirathna T Asaeda B L S Thilakarathne andH Kadono ldquoNanometer-scale elongation rate fluctuations intheMyriophyllum aquaticum (Parrot feather) stem were alteredby radio-frequency electromagnetic radiationrdquo Plant Signalingand Behavior vol 9 no 4 Article ID e28590 2014

[56] M Ursache G Mindru D E Creanga F M Tufescu and CGoiceanu ldquoThe effects of high frequency electromagnetic waveson the vegetalrdquo Romanian Journal of Physics vol 5 no 1-2 pp133ndash145 2009

[57] E A M Hamada ldquoEffects of microwave treatment on growthphotosynthetic pigments and some metabolites of wheatrdquoBiologia Plantarum vol 51 no 2 pp 343ndash345 2007

[58] M D H J Senavirathna A Takashi and Y Kimura ldquoShort-duration exposure to radiofrequency electromagnetic radia-tion alters the chlorophyll fluorescence of duckweeds (Lemnaminor)rdquo Electromagnetic Biology and Medicine vol 33 no 4pp 327ndash334 2014

[59] Y Shckorbatov ldquoThe main approaches of studying the mech-anisms of action of artificial electromagnetic fields on cellrdquoJournal of Electrical amp Electronic Systems vol 3 no 2 2014

[60] A M Pietak ldquoStructural evidence for electromagnetic reso-nance in plant morphogenesisrdquo BioSystems vol 109 no 3 pp367ndash380 2012

[61] AAmat J Rigau RWWaynant I K Ilev and J J Anders ldquoTheelectric field induced by light can explain cellular responses toelectromagnetic energy a hypothesis of mechanismrdquo Journal ofPhotochemistry and Photobiology B Biology vol 82 no 2 pp152ndash160 2006

[62] Z Qiu J Li Y Zhang Z Bi and H Wei ldquoMicrowavepretreatment can enhance tolerance ofwheat seedlings toCdCl

2

stressrdquo Ecotoxicology and Environmental Safety vol 74 no 4pp 820ndash825 2011

[63] Y-P Chen ldquoMicrowave treatment of eight seconds protectscells of Isatis indigotica from enhancedUV-B radiation lesionsrdquoPhotochemistry and Photobiology vol 82 no 2 pp 503ndash5072006

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

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Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

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Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


120582

rarr

E

rarr

BDOP

(a) (b)

(c)

Rotating stirrer

Emitting antenna

Specialized plantculture chamber

(d)

Figure 1 Electromagnetic wave and experimental set-up (a) Schematic representation of an electromagnetic plane wave showing thetransverse and space varying electric (119864) and magnetic field (119861) The wavelength (120582) is the distance between two crests DOP directionof propagation (b) A TEM cell (transverse electromagnetic cell) (c) A GTEM cell (gigahertz transverse electromagnetic cell) (d) MSRC(mode stirred reverberation chamber) Note the double-sided metallic walls the emitting antenna the rotating stirrer and the specializedculture chamber that stands in the ldquoworking volumerdquo where the electromagnetic field characteristics have been extensively characterized

achieve genetically stable plant lines through the selection ofspecies that favor asexual reproduction [4] or self-pollination[5] Furthermore metabolic mutants are easily available forseveral species and constitute invaluable tools to understandthe way the EMF signal is transduced [6] Indeed severalreports have pointed out that plants actually perceive HF-EMF of even small amplitudes and transduce them intomolecular responses andor alterations of their developmen-tal scheme [3ndash9] The way that HF-EMF interact with plantsremains essentially unanswered However since EMF evokea multitude of responses in plants they might be consideredas a genuine environmental stimulus Indeed EMF exposurealters the activity of several enzymes including those ofreactive oxygen species (ROS) metabolism [7] a well-knownmarker of plant responses to various kinds of environmentalfactors EMF exposure also evokes the expression of specificgenes previously implicated in plant responses to wounding[5 8] and modifies the development of plants [9] Fur-thermore these responses are systemic insofar as exposureof only a small region of a plant results in almost imme-diate molecular responses throughout the plant [6] Theseresponses were abolished in the presence of calcium chelators[6] or inhibitors of oxidative phosphorylation [10] whichimplies the involvement of ATP pools In the present reviewwe describe exposure devices SAR determination methodsand biological responses (at both the cellularmolecular andwhole plant levels) observed after plant exposure to EMFWefocused this review on radiated (ie EMF that are emitted

through an antenna) HF-EMF (mainly within the rangeof 300MHzndash3GHz) and consequently will not address thebiological effects of static magnetic fields (SMF) extremelylow frequency electromagnetic fields (ELF) or HF currentinjection since their inherent physical properties are dramat-ically different from those of high frequencies Therefore theHF-EMF we consider should be viewed through the prismof classical electromagnetism macroscopic electrodynamicsphenomena described in terms of vector and scalar fields

2 Exposure Systems and Dosimetry

HF-EMF are a combination of an electric field and amagneticfield governed by Maxwellrsquos equations At high frequencythese vector quantities are coupled and obey wave equationswhether for propagating waves or for standing waves Invacuum the former travel at the speed of light (asymp3sdot108msminus1)and have the structure of a plane wave (Figure 1(a)) In othermedia the speed decreases and the spatial distribution for theelectric and the magnetic fields are generally arbitrary (thusnot being a plane wave) The latter which do not propagatebut vibrate up and down in place appear in some particularconditions (eg bounded medium like metallic cavity) andplay important roles inmany physical applications (resonatorwaveguide etc)

In both cases HF-EMF are characterized by an amplitudeof the electric (119864) or magnetic (119867) components (measuredin volts or amperes per meter) a frequency 119891 (number of



120582 =

119888

119891

= 119888 times 119879 (1)





119875119894=

1198642

2 times 1198850

(2)




119875119889 =∭

V

120590 times 1198642

2

119889119881 (3)













SAR = 119889119889119905

(

119889119882

120588 times 119889119881

) =

120590 times 1198642

2 times 120588

(4)


SAR = 119862 times (119889119879119889119905

)

119905rarr0

(5)














[28]











2O2





5-fold) [7]

MDA and H2O2content







[18 27]



Triticum aestivum









30 resp) [30]








respectively























[36]



[36]


[36]


[36]


[36]



[36]












(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



120582 =

119888

119891

= 119888 times 119879 (1)





119875119894=

1198642

2 times 1198850

(2)




119875119889 =∭

V

120590 times 1198642

2

119889119881 (3)













SAR = 119889119889119905

(

119889119882

120588 times 119889119881

) =

120590 times 1198642

2 times 120588

(4)


SAR = 119862 times (119889119879119889119905

)

119905rarr0

(5)














[28]











2O2





5-fold) [7]

MDA and H2O2content







[18 27]



Triticum aestivum









30 resp) [30]








respectively























[36]



[36]


[36]


[36]


[36]



[36]












(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology







SAR = 119889119889119905

(

119889119882

120588 times 119889119881

) =

120590 times 1198642

2 times 120588

(4)


SAR = 119862 times (119889119879119889119905

)

119905rarr0

(5)














[28]











2O2





5-fold) [7]

MDA and H2O2content







[18 27]



Triticum aestivum









30 resp) [30]








respectively























[36]



[36]


[36]


[36]


[36]



[36]












(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










[28]











2O2





5-fold) [7]

MDA and H2O2content







[18 27]



Triticum aestivum









30 resp) [30]








respectively























[36]



[36]


[36]


[36]


[36]



[36]












(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology
















[36]



[36]


[36]


[36]


[36]



[36]












(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








(52) [38]



reduced by 43 [27]

























0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


0

2

4

6

8

C

Calm-n6Lecdpk1Pin2

5 15

lowast

lowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

lowastlowast

lowast

lowast


0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(d) EGTA (05mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(e) BAPTA (04mM)

0

2

4

6

8

C 5 15

Calm-n6Lecdpk1Pin2

(f) LaCl3 (01mM)




0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


0

5

10

15

20

60

Shielded

C 15 30

Treated

lowastlowast

(a)

00

02

04

06

08

10

60C 15 30

ShieldedTreated

lowast

(b)


Pin2

mRN

A ac

cum

ulat

ion

Terminal leafC

8

7

6

5

4

3

2

1

00 15 C 0 15

Leaf 1(a)

Pin2

mRN

A ac

cum

ulat

ion

8

7

6

5

4

3

2

1

0C 0 15 C 0 15















2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










2[62] or UV [63]




Acknowledgments


References



































































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



















































2










Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Review Article Plant Responses to High Frequency...

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Transcript of Review Article Plant Responses to High Frequency...