Agric. Rev., 27 (4) : 235 - 246, 2006

, ROLE OF CALCIUM IN THE PHYSIOLOGYOF PLANTS - A REVIEW

Ritu JhaInstitute of Agricultural Sciences

Banaras Hindu University, Varanasi - 221 005, India

ABSTRACTThe physiology of plants is undoubtedly affected bya nwnber of elements directly or indirectly.

The importance of calciwn as an essential rnacronutrient in the functioning of plants is inevitable. Itis the criticaJ role of calcium in influencing the working of the plant system that obviously attractedthe attention of a nwnber of research workers around the globe.

J

Calcium is an iUlportant apoplastic (inplant cell walls and membrane) andsymplastic(as a second messanger) nutrient(Zocchi et a/., 1995). It has a crucial role toplay in dealing with several physiologicaldisorders, firmness retention, protecting theplants against salinity stress, callus friability andsomatic embryogenesis (Montoro et aJ., 1995),flower induction and quality, solublepolyuronides content, middle lamella retentionand formation. It is necessary for normalmitosis and is an important activator of severalenzymes, important for carbohydratetranslocation, prevents chlorosis in the youngerleaves; peel pitting and cuticular waterpermeability. Since the recent discovery ofCalmodulin it has become clear that calciumis not just a rriacronutrient but' also a majorcontroller of plant metabolism anddevelopment.

Calcium was once consideredimportant only f9r cell wall structure, butQuality refers to several aspects, which affectthe marketability of the product, and includesattractiveness, organoleptic, nutritional value,intact state and shelf life. All the above factorssuggest the crucial role of calcium inmaintaining the quality of the agriculturalproducts (Saha etaJ., 1998; Han et a/., 1990).

The objective of the present reviewwork is to deal briefly with the ability of calciumto prevent or to alleviate a wide variety of stressconditions, to anticipate and relieve

physiological, environmental and mechanicalstresses, in bringing about structural firmnessand the effect of preharvest application ofcalcium on the storability of the products.

It is expected that the present reviewwork will ~ helpful in bringing the scatteredinformation in a concise form and extendfurther research work in this promising field.REQUIREMENT AND EFFECTS OF HIGHCALCIUM SUPPLY IN THE PLANTSYSTEM

Calcium is taken passively by the plantsystem. It is transported by the transpirationalwater flow. So, all the low transpiring organssuch as fruits (apples, tomatoes, sweetpeppers), tubers (potatoes), covered leaves(inner leaves of lettuce, Chinese cabbage),flower buds, storage tissues etc of the plantsare most affected by the calcium deficiencysymptoms (details in Section 5).

. Higher levels of calcium are requiredwhere:1. Yield levels and crop growth rate are high,

high removal of nutrients by crop.2. Levels of NH/, K+, Mg++ are high

(antagonism).3. Root growth is limited/reduced due to soil

temperature, soil structure, soil watercontent.

4. Water uptake is reduced under varyingconditions;· drought, high salt levels in soilor in water.

Some of the effects of high calcium

236 AGRICULTURALREVl~S

on the functioning of the plant system are~s respecUvely. rh~·CC(fh.tx to tl1e xylem tl1roughfollows:- . the apoplask pathway Is influenced markl?dly1. High calcium supply~esists some diSl?ases by transpiration, which could" lead,y~·vagaries

better (Gislerod, 1999HBar·Tal et at, 2001) in the amount of Casupplied to the shoot and2. Plants tolerate tl9nsport better due to firmer development of Ca disorders (White and

cell wall (Siddiqui and6angerth,. 1996; Broadly, 2003). The basic mechanism ofTzoutzoukou and Bouranis,.1997j Tomala, calcium is to work as a computing center in1997). . . .. ... . . ... whi2hall signals of the hormones are calculated

3. Higher levels of lycopene andyitamln C andacomplex actis initiated.(Baslouny, 1994).. RQtEOF CALCIUM IN RECOVERY

4. Plants tolerate high. and low temperature AGAlNSTDlFFERENT ENVIRONMENTALstresSeS· as transpiration is improved STRESSES(Tahtiharju et a/., 1997, 20(1). Calcium Ions fundi~n as intracellular

5. High calcium concentration mitigates tfw sec()hd messengers in regulating a plethora ofadverse effects of salinityonplantwowth cellular processes from acdimative stress(YounisetaJ., 1994; Maksoud ttai., 1995}. responses·to survival and programmed ceU

MECHANISM OF ACTION OFCa2+: death (NG. KY Carl.et a/., 2003)..CaJci,um ion has a .vital role In . ... Calcium plays a major role in

mediating plant response to external stimuli mediating stress response during injUry,of both abiotic origin (e.g. light,cold, heat, recovery from injury and acclimation to stress.movement, hypoxia and drought) and biotic Ca2+ Is necessary for recovery from freezeorigin (e.g. phytohormones, pathogen, Injury by activating the plasma membraneinteractions with symbionts). It has been shown enzyme ATPase which is required'to pumpthat plasma membrane Ca2+channels and backthe nutrients that were lost incell damage.vacuolar Ca2+release channels may participate Dealing with the impact of calciumin multiple signaling pathways in higher plants. and protein phosphatase in cold signalCa2+dependent modulation of cellularbinding transduction In Arabidopsis thaliana, Tahtiharjuproteins, of which calmodulin is one of the etal. (1997, 2001) reported that Ca2+best characterized. In terms of plant growth mediated cold signal transduction Is a complexthe ge'he DWF1 and Ca works with a process which involves an increase in cytosoliccalmodulin. The Ca loaded Calmodulin can Ca 2+levels through the action of bothbind to and change the conformation and plasmalemma and tonoplast Ca2+channels andactivity of its target proteins such as DWFl. It transduction of this· signal via various coldis well documentedthatCaisinVol\l~dirtligl1t upregulated Ca2+binding proteins tOthel~velinducedphytochrom~centrall~d~i9nal ofgene expression; .. •.. ,transduction pathways In higher plants (Tretyn, Lopez and Satti (1996) studied the1999). . effects of salinity on yield of tomato under

A number of research studies suggest sodium chloride stress and the importance ofthat Ca might reach the xylem solely via the calcium and potassium In preventing it. It wasapoplast in regions where the casparian band reported that the addition of Ca and potassiumis abse~nt or disrupted or circumvent the either alone or In combination to the salinecasparian band by entering the cytoplasm of nutrient solution increased root volume, freshuns/-lberized endodermal cells· when the weight, Ca concentration, leaf fresh weight andcasparian band Is present. These are referred fruit yield pf'r plant.to ils apoplastic and sympla~tic pathways Younls et a/. (1994) investigated the

VoL 27. No.4, 2006 237

combined effects of salinity and Ca(N03)z or maintaining an intact middle lamella might notKN03 0n growth and metabolism of Phaseolus be its direct ionic effect (Siddiqui and Bangerth,vulgaris and concluded that CaZ+ or K+ addition 1996; 6rown" et al., 1998).to a saline nutrient solution improved plant i'; ',lnasirnilcirexperiment itwas obselVedmetabolism (reducing sugar .andsucrose thatl.2%'CaCl~CltweeklyinteIVals and aftercontent, polysaccharide content and" protein fhreeWeeksofstorage both average and smallcontent). Similarly Crameret al. (1990), truitswereshowingbetterretention offirmnessMaksoud et al. (1995) and Caines et al. (1999) by CaCl2treatment The result was discussedstudied the effect of CaS04 applica~ion in in relation tocell wall yield, p-Dgalactosidasemitigating the adverse effects of saliriityon activitY,total free" ionicaltyassociuted andplant growth.- covalently, bound pectins and hemicellulose

Sylvia Lindberg, 2001 studied the rote contents. The difference.in behavior of averageof Ca and ph in stress signalingandjl1~UXin and small fruits to calcium application seemssigpal transduction in plant cells. It was noticeo to be associated with the Ca.

_ that when plants were subjected t() different Furi:her investigations on differerttial- types of stresses,.suthassalt, cold,mechanicaleffecfofcalcium" and', strontium on flesh

and aluminium stress, the stress induces a fast firmness andproperties of cell walls in apples,often transient increase in Ca concentration led to the conclusion that preharvestin the cell cytosol. Change in cytosolic Caz+is application of CaClzmay not always lead tooften related with a change in cytosolic ph. firmer fruits at the time of halVest but mayThe aim of the work was to clarify the result in a better retention of firmness duringmechanism of calcium. , - storage. It was further indicated that the effectROLE OF'C'ALCIUM IN BRINGING ofCa on f1eshflrmnessand cell wall propertiesABOUT S11lUCTURAL FlRMN~l>. ,,' was not simply electrostatic or of a bivalent

Stow (1996) studied the" eff~ct or clItion but through some sp~cific effect.calcium iorts on apple fruitsqft~ning durJng ." Different formulations of Ca werestorage and ripening. 1t was reportedthafapple , applied to treesofthe apple cultivar Sampionfruit softening resuljs from loss,of cal~ium from 'in a commerCial orchard and it was studtedioniclinkages betweenpectin molecules'in the that all theti"eatments".decreased internalmiddle lamella. this result was tested by ethylene, reduced starch degradation andinfiltration of apple fruit tissues (cultivars Cox's usually increased fruit firmness (fomala, 1997).orange Pippin, Bramley's Seedling and Gloster Ge'rasopoulos et al. (1996) studied the69) with calcium acetate solution. Infiltration effects of the spray of "kiwifruits cv. Haywardpartially reversed softening ihat had~esulted with CaClzano concluded that CaClz spraysfrom delayed harvesting, storage in air or usually increased fruit pericarp, core and skin1.25% 02 at 3.5°C and ripening at lOoC in Ca by at least 200%' and increased firmnessair. and titrable aCidity but decreased soluble solids.

The iRfiltration of Apple cv. Golden "Ina similar work Gerasopoulos andDelicious with 150 mM CaClz resulted in the Richardson, 1996 worked on'theeffects ofhigher reduction of flesh firmness throughout exogenous propylene andjruit calciul11 onthe storage period but with 50 mMCaClzthis ripening of non-chilled and chilled Anjou peatscould be retained only up to" 25 days. The and condudedfhat the" Ca uptake was""content of insoluble, calcium' in the flesh significant only when high concentrations were'increased "with increase in storage period. 'It applied. The high Ca fruttssbowed consistentlywas concluded that the effect of Ca -in betterfirmness retention and a slower increase

238 AGRICULTURAL REVIEWS

in internal ethylene.CALCIUM DEACIENCY SYMPTOMS INPLANTS

Excess of Ca ions are generallyconsidered non-toxic to plant organs(Marschner, 1986). Calcium nutrition becomesa major consideration where natural level ofcalcium is low (soil types, sand and substrates).Blossom end rot (BER):

Paiva et al. studied the effect of variousconcentrations of Ca in the nutrient solutionof hydroponically grown tomatoes (cv. Jumbo)and concluded that increased Ca concentrationin the nutrient solution has its effect on Mg,lycopene, carotene and K concentrations astheir levels decreased.

Similar investigations were carried outon tomato cv. Diva (Plese et al., 1998) and itwas concluded that the foliar application ofCa reduced the percentage of blossom end rot(BER) to a minimum. L.C. Ho et al. reportedthat neither Ca-efficiency nor a high Ca uptakeis a sound basis for the selection of tomatocultivars for resistance'to BER. The crucialfactor is the ability to divert sufficient Ca awayfrom the leaves to the tissues and particularlyto the distal part of the fruit. Low Ca, P andhumidity results in higher incidences of BERthan the higher levels of these factors (Kreij,1996) (Franco et al., 1998) (Wada and Ikedaet al., 1996) (Bar-Tal et al., 2001). It isrecommended that at least a Ca concentrationof 8-9 mM can avoid BER. Marcelis et al.discussed the usefulness of the total Caconcentration of fruits for determining thecritical Ca concentration in the induction ofBER in fruits of Capsicum annuum L. andreported that pericarp Ca concentration ofmature fruits is negatively related to both fruitsize and BER incidence.Peel pitting and bitter pit:

Calcium nitrate reduces peel-pittingand cuticular water permeability of 'Fortune'mandarin when applied just before or at fruitcolor break (Zaragoza et al., 1996). 33 to 81%

reduction in fruit break was observed. Injectionof 1% and 2% CaCI2 solutions into the corecavities of harvested fruits of apple cvBramley's Seedling apples at harvest reducedthe bitter pit disorder in the stored fruits from32% to 16% and 5% respectively (Perring andPearson, 1987t,

. In a similar investigation leaf calciumcontent and the incidence of bitter pit werenegatively correlated in the Gala, GoldenDeliCious and Fuji cultivars of apple (Nachtigallet al., 1998). Similarly, fruit Ca content (on adi-y weight basis) 14 weeks after full bloomand the incidence of bitter pit was negativelycorrelated in Golden Delicious and Ca contentin the peel 14 weeks after full bloom wasnegatively correlated in Golden Delicious andFuji, respectively. It was concluded that thebitter pit incidence could be predicted by Cacontents of leaves and fruits at harvest.

When investigations were carried outon Sundale Spur Golden Delicious it wasreported that spraying with CaCI2, slightlyreduced bitter pit, increased fruit Ca content,reduced fruit Mg content and increased thenumber of fruits per spur (Witney et aJ., 1991;Grange et aJ., 1998). Along with several otherfactors bitter pit is significantly related to Cadeficiency in the plant system (Juan et al.,1997; Uu Hui Chao and Han Zhen Hai, 1997;Vaysse et al., 2001).

Dris et al. (1998) studied the role ofnitrogen and calcium nutrition and fruit qualityof commercial apple cultivars grown in Rnlandand reported that fruits with Ca content below45 mg kg'! fresh weight were susceptible tobitter pit (Aroma and Akero) and Jonathan spot(Red Atlas).Bract distortion and bract necrosis:

When experiments were carried outto determine the effect of direct Ca sprays onthe distribution and binding of Ca in the leavesand the severity of leaf/bract distortion in thetwo varieties of Euphorbia puJcherimma Willd,distortion susceptible N-14 Glory) and non-

Vol. 27, No.4, 2006 239

susceptible ('Annette Hegg Dark Red', AHDR)cultivars were applied with 100 mg I-lor 400mg 1-1 of Ca. EDX analysis suggested thatdistorted regions of V-14 leaves and bracts hadlower Cac;oncentrations than did undistortedregions or AHDR leaves and these deficienciescan be partially overcome by weekly Ca sprayapplication (Daniel. J. Jacques et al., 1991).

Similar work was conducted to studythe effect of 2, 3, 5-triiodobenzoic acid on Calevel in two inbred lines and eight cutivars ofsunflower (Helianthus annuus, L). It wasconc1Jded that TIBA produces both bractnecrosis and lower Ca content in bracts. It wassuggested that bract necrosis is a physiological,disorder related to Ca deficiency under stresscondition (Guardia, M.D. de la. et a/., 1990).Browning and black patch:

In a field experiment conducted ongrapes cv. Waltham Cross and it was observedthat 0.69 and 0.92% calcium treatmentsreduced browning to 0% (Strydom, G.J. eta/.,1999).

The effect of Ca in the progression ofthe vascular browning of the roots by f solani,which led to the Piper bettie cv. Ponnus-Sdecline in Andhra Pradesh, India, was studied(Lakshmi et al., 1997). It was concluded thatas the concentration of Ca increased, theactivities of polygalacturonase and pectinmethyl esterase in f solani colonized rootsdecreased, thereby reducing the diseasesymptoms. The effect of foliar application ofCaCI2 on the abnormal fermentation oforiental melon (cv. Gumssaragi-eunchun) wasinvestigated (Chung Hee Don et aI., 1998) andit was reported that CaCl2 inhibited theoccurrence of abnormally fermented fruitswhen applied 3 times at 5 days intervalsfrom10 days after flowering (Daniel. J. Jacques etal.,1991).Skin bursting, side rot, tip burn and scab:

Kreij, 1990 studied the effect of Caon skin bursting and concluded that thepercentage of affected fruits at the lowest Ca

rate amounted to 37% compared to only 14%in the other Ca treatments.

Internaltipburnof cabbage is a seriousquality defect caused due to calcium transportcharacteristics within the plant. The effect ofcalcium nutrition and cultivar in bringing abouttipburn of Collard was studied (Johnson,1991).

Investigations conclude that calciumchloride reduces the incidence of side rot inBose pears (Sugar et a/., 1992). At 6.0 g/litreof calcium, the mean area of decay wasreduced at spore concn > 1021m!. CaClztreatment reduced incidence of side rot innaturally infected fruit in 3 yr of trial.

Montag-et al. (2005) studied thesuitability of· hydrated lime for stop-spraystrategies against apple scab (Venturiainaequalis) and concluded that suspensions ofcalcium carbonate (6.75 g/l) had no effect oncuticular penetration of the fungus.EFFECT OF PRESTORAGE ANDPREHARVEST APPLICATION OFCALCIUM ON YIELD

Results of several previous workssuggest that nutritional management inconjugation with other methods can play acru~ial role in postharvest decay control,enhancement in yield and quality (Tzoutzoukouand Bouranis, 1997; Gerasopoulose et al.,1996; Roose, 1999; De Ell, etal., 2000).

When calcium formulations Ca EDTAand Nutrical were applied to rabbiteyeblueberry cv. Tifblue, bushes at different ratesboth Ca formulations and paclobutrazolproduced significantly firmer berries attharvestand this firmness was markedly maintainedafter 2 weeks' storage compared to the control.TSS decreased during storage and was greatestin the control fruits while total acidity washigher in Ca treated fruits compared withpaclobutrazol treated fruits or the control fruits.

Sugar et a/. worked on themanagement of nitrogen and calcium in pear :trees for enhancement of fruit resistance to

240 AGRICULTURAL REVIEWS

postharvest decay and concluded that low N parenchyma increased and extended bundleconcentration and high Ca fruit content aimed sheath formation decreased at the adaxial sideat reducing the severity of postharvest fungal of minor veins of the leaves, as compared todecay and are additive factors in decay the leaves of plants grown with a higher Careduction. Chung Hee Don et a1. (1995) supply. It was concluded that the Ca ioninvestigated the effect of CaCl2 foliar induced additional cell divisions. in the bundleapplication on membrane protein profiles and sheath extensions and that a high supply of,cell wall structure of strawberry plants (cv. Ca led to the formation of a second type ofYeohong). It .was observed that 'the foliar crystal in the bundle sheath.application of CaCl2did 'not affect the soluble TretYn et aJ. (1994) reported thatanprotein content and protein band patterns of increase in free Ca ions, the calciumfruits but did induce the production of a new ionophores A 23187 and ionomycin andmembrane protein, MW 89 k Da. It was .' caffeine before and during the first 2 hrs ofobserved that the fruits obtained from CaCl2 the dark period stimulated flowering oftreated plants stored for 12 days at 5°C, had Pharbitis nil cv. Violet whereas after the 6th

a distinct middle lamella which was absent in hour" it decreases. It was postulated that thecells from control fruits. tar6ets for Ca action are stomata, which are

Raike and Red Atlas apple trees were open before the dark period and remain closed ;-sprayed 6 times with CaCl2(1.3g/litre) -at dUring the first 4-5 hours of the dark period.fortnightly intervals. Dris and Niskanen, 1998 The IAA induced leaflet 6pening,put forward that Ca treatment increased fruit which occurs in darkness in the flo~rs of C.N and decreased fruit P content. fasciculate, was inhibited by tM Ca2+ chelator

Xiao Yan et al. (1998) studied the EGTAor by antagonists. In contrast it waseffect of preharvest spraying Ca and NAA on reported -that··the 1AA induced opening wasstorage of strawberry cv. Hani by applying enhanced by ionophore A 23187Ca(N0:J2 + NAA at 10 mg/litre as foliar spray (Bourbouloux et a/., 1992).to the plants and concluded that the fruit rot Phaseolus ,coccineus -cv. Pieny Jasindices of frUits treated with Ca(N03)2 at seedlings were grown in Knop solution at low1.0,0.5, 1.5, 0.2 and 0% (control) were 40, (85 mg litre-I), medium (170 mg) or high (25558,82,100 and 100% respectively. mg) rates ofCa and given 25 ~M Cd upon

In the greenhouse trials carried out in transfer and after 10 days. Skorzynska et al.Espirito San~o do Pinhal, SP Brazil in 1993 (1998) reported that in younger plants glucoseand 1994, tomato plants were supplied with accumulation in leaves decreased as Ca in thevarious combinations of NPK, dolomite, boron culture solution increased and with Cdor Ca (0.6%CaCI2). (;a and dolomite treatment. it was observed that the glucoseapplicatioTt both reduced the percentage of content decreased at low and medium Ca andfruits with stylar decay (Olivwia et aJ., 1995; increased at high Ca. Cd treatment increasedAnderson -and Campbell, 1995). , plant sucrose content, but this effect decreasedPHYSIOLOGICAL EFFECTOF CALCIUM as Ca rate increased. 'ON THE PLANT SYSTEM Calcium application has its direct role

.Investigations were carried out on the in enhancing the growth of plants (Leonardplants of P. vulgariS grown in nutrient solutions and Hepler, 1990). The growth of C. pepoat different levels of Ca concentration.Zindler- cv. Kueta (Wui and Takano, 1995) seedlings,Frank, 1995 reported that when Ca grown in full Knop's nutrient solution wasconcentration was low the amount of palisade studied for 10 days after germination and it,

Vol. 27, No.4. 2006 241

-- .

was reported that the maximum growth rate messenger system operates between thein the Ca deficient solution was only 43% of plasma membrane and calcium ionthat in the full nutrient solution. sequestering organelIes. The endogenous

The degree of correlation was studied growth regulator abscisic acid elevated cytosolicbetween the mineral elements and reducing calcium ion levels in a minority of cellssugar in pistachio. A positive correlation was investigated, even though stomatal closurestudied between the Ca content in the leaves always occurred. Calcium ion dependent andand the amount of reducing sugar (Idem et al., independent pathways linking abscisic acid1995). This specified the role of Ca in the perception to stomatal closure were thusreducing sugar synthesis in plants. investigated.

Ca is a second messenger, which binds Maffei et al. (2004) studied theto the protein calmodulin found in the cytosol membrane potential and intracellular calciumof plant cells. A number of metabolic processes variations in Lima bean (Phaseolus lunatus)are regulat.ed by Ca-ealmodulin -complex leaves when the Mediterranean climbing(Hepler and Wayme, 1985). cutworm (Spodoptera littoralis) was attacking

Xu Haixin et al. (1998) investigated the plants. The involvement of calcium ions into role of cytosolic free Ca ([Ca2 +)) in the signaling after herbivore ~nding is discussed.hypersensitive response of cowpea to the The influence of Na CI and Ca Cioncowpea rust fungus. A slow prolonged growth, ion accumulation and prolineelevation of ([Ca2 +]) in epidermal cells of accumulation was investig-aJed in cellresistant but not susceptible plants was noticed suspension culture ofrice (OlYza sativa L). Theas the fungus grew through the celI wall. relative growth rate of suspensions wasElevated ([Ca2 +J) level represents the first sign significantly greater at high Ca level (5.0 m M)of hypersensitive response detectable in the than at low (0.5 m M) in response to 150 m Mcowpea rust fungus system. It is also related to Na Cl. The proline level of cells increased inthe stage of fungal growth and notto the speed response to Na Cl but the Increase was 4-9of Initiation of subsequent cell death. fold at high and 1-4 fold at low Ca level

NG. K.Y Carl et aJ. (2003) in their respectively (Safdar Hussain Shah Satoshistudies investigated the encoding specificity in et al., 2001).plant calcium signaling and how stimulus . There are more than 1,65,000specific information can be encoded in the websites dealing with role of calcium in theform of Ca2+ signatures. physiology of plants. Appendix I presents the

Plasma membrane depolarization list of a few websites reporting the recentinduced by ABA in Arabidopsis Suspension research work on the role of calcium in theCells involves reduction of proton pumping in physiology of plants.addition to anion channel activation which are SCOPEFOR FURTHER INVESTIGATIONSboth Ca2+ dependent (Brault, M.et al., 2004). Presently a number are tnvestigators

Cytosolic abscisic acid activates guard are investigating the role of calcium and Ca ~ .cell anion channels without preceding Ca2+ binding proteins in the control of growth andsignals (Levchenko, V. et al., 2005). gravitropism. Evidence suggests that Ca plays

.' Gilroy, S. et aI. (2000) studied the role a major role in regulating a number ofof cytosolic calcium ions In signal transduction interrelated processes intril1sic to cellularof somatal guard cells of Comme/ina communis- expansion, division and orientation.using fluorescence ration imaging and Still controversy -exists about thephotometry. It was concluded that a s~c;ond ~~ulatory role of Ca orraspatfate kinase (AK)

242 AGRICULTURAL REVIEWS

activity in plants, such as regulation of Caenzymes involved in lysine catabolism (Kemperet a/., 1998; Gaziola et aI., 2000).

. Several genes have been cloned andcharacterized that encode for Calmodulin(CaM)- binding proteins. The primary goal ofresearch is to investigate the functionalsignificance of these genes and understand howthey are involved in Ca2+/CaM mediatedsignaling.

One aspect of plant Ca2+ signaling that

is currently attracting a great deal of interest ishow Ca2+ signature's specific spatio temporalchanges in cytosolic free Ca2+ and encode thenecessary information (NG. K.Y. Carl et a/.,2003).

ACKNOWLEDGEMENTAuthor is very much thankful to Prof.

S.P. Singh, Institute of Agricultural Sciences,Banaras Hindu University for his valuablesuggestions on the subject.

REFERENCESAdams, J.E and Hartzog, D.L. (1991). J. Pl. Nutr., 14: 841-851.Adams, P. and Ho, L.C. (1989). J. Hart. Sci., 64: 725-732.Akhawan-Kharazian et al. (1991). Arid Soil Res. Rehabilitation,S: 97-103.Anderson, J.L. and Campbell, W.E (1995). Acta. Hort., 398: 47-57.Bach, M. et al. (1993). Plant Physiol., 103: 407-412. •Bandzaitiene, Z. (2000). Sodininkyste ir Darzininkyste, 19: 256-263.Bar-Tal, A et al. (2001). Acta. Hort., 554: 97-104:Bar-Tal, A et al. (2001). Agronomie., 21: 393-402.Basiouny. EM. {1994). Acta. Hort., 398: 893-900.Beel, E. and Bruyn, P.D.E. (1998). Verbondsnieuws., 42: 31-33.Boselli, M. and Volpe, B. (1990). Rivista di Viticoltura e di Enologia, 43: 43-54.Bourbouloux, A etal. {1992). J. Exp. Bot., 43: 63-71.Bramble, J.L. and Graves, D.J. (1991). Biotechnol and Bioengineering, 37: 859-868.Brault, M. et al. (2004). Plant Physiol., 135: 231-243.Brown, G. et al. (1995). Scientia Hart., 62: 75-80.Brown, G.S. etaJ. (1998). Acta. Hart., 464: 41-46.Buerkert, A and Marschner, H. (1992). Plant. Soil, 147: 293-303.Caines, AM. and Shennan, C. (1999). Plant Physiol. Biochem. (Paris), 37: 569-576.Caines, A.M. and Shennan, C. (1999). Plant Physiol. Biochem. (Paris), 37: 559-567.Canini, A et al. (2001). Plant Biosystems, 135: 123-132.Cardoso, M.O. et al. (1995). Hort. Brasileira., 13: 172-175.Casero, T. (1996). ITEA Production Vegetal, 92: 58-63.Chen You Zhi etal. (1998). J. Arner. Soc. Agric. Sci., 123: 524-531.Chow, K.K. et al. (1992). Scient/a Hort., 95-104.Chung Hee Don et al. (1995). J. Korean Soc. Hart. Sci., 36: 486-492.Chung Hee Don et al. (1998). Korean J. Hort. Sci. Technol., 16: 215-218.Conway, W.S. et al. (1994). Hort Technol., 4: 239-243.Cramer, GRetal. (1990). J. Pl. Nutr., 13: 1453-1462.Daniel. J. Jacques et al. (1991). J. PI. Nutr., 14: 637-652David Braver et al. (1991). J. PI. Nutr., 14: 729-740.David Braver (1994). J. Pl. Nutr., 17: 709-716.Dawson, D.M. et al. (1993). Postharvest BioI. Technol., 3: 131-141.De Ell, J.R. et al. (2000). New England Fruit Meetings, 106: 43-46.Dey, J.K. and Singha, D.O. (1998). Indian J. Agric. Sci., 68: 139-143.Dhru Pal (1991). Adv. Plant Sci., 4: 264-267.Doneche. B. and Chardonnet, C. (1992). Vitis., 31: 175-181.Dong Cai Xia et al. (2001). Acta. Hort., 28 (Supplement).Oris et al. (1998). J. Pl. Nutr., 21: 2389-2402.Faiz, S.MA et al. (1994). Curro Agric., 18: 9-12.Fernandez et aI. (1998). Acta. Hort., 468: 683-689.

Vol. 27, No.4, 2006 ,- 243Franco, JA et a/. (1998). Revista de Horta/izas, Flores, Plantas Ornamentales y Viveros.. 126: 90-92.Freyssac, V. eta/. (1999). Acta. Hort., 494: 167-17I.Galiola et aI. (2000). Physio/. Plant, 110: 164-17I.Gerasopoulos, D. et a/. (1996). Postharvest Bioi. Techno/., 7: 65-72.Gerasopoulos, D. and Richardson, D.G. (1996). Postharvest Bioi. Techno/., 8: 111-120.Gilroy, S. et a/. (2000). Plant Cell., 3: 333-344.Gislerod, H.R. (1999). Acta. Hart., 481: 345-352.Grange, SA LE et a/. (1998). J. Southern African Society Hart. 5.::i., 8: 5-9.Guardia, M.D. de la eta/. (1990). J. PI. Nutr., 13: 117-129.Gunes, A. and Post, W.HK (1995). Turkish J. Agri. Forestry, 19: 179-183.Guzman Estrada, C. et al. (1998). Revista de la Facutad de Agronomia, Universidad Central de Venezuela, 24: 41-58.Han Wen Van and Xu Yun Wen (1996). J. Tea Sci., 16: 13-18.Han, Z.H. et a/. (1990). J. PI. Nutr., 13: 1155-1166.Hicklenton, P.R and Cairns, R.G. (1992). J. Environ. Hart., 10: 104-107.Ho, L.C. (1988). Applied Agri. Res., 3: 275-281.Huang, J. and Redmann, RE. (1995). J. PI. Nutr., 18: 1371-1389.

.Hush, J.M. et aI. (1991). Plant, Cell and Environ., 14: 657-665.Idem, G. et a/. (1995). Acta Hort., 419: 329-333.J.M. Penalosa eta/. (1994). J. PI. Nutr., 17: 147-153.Jan E. Mikesell (1994). J. PI Nutr., 15: 1323-1341.Jager, A.DE (1996). Fruitteelt (Den Haag), 86: 12-13.Jo Jonghyeon et a/. (1995). RDA J. Agric. Sci., 37: 283-290.Johnson, J.R. (1991). J. Amer. Soc. Hort. Sci., 116: 991-994.Johnson, J.R. (1991). Hort. Sci., 26: 544-546.Jones, H.G. etaI. (1986). J. Hart. Sci., 61: 171-179.Juan, J.L. et aJ. (1997). Acta. Hart., 448: 273-282.Kaya, C. et aJ. (2002). Sci. Hart., 93: 65-74.Keifer, A.Q. etaJ. (1992). Planta., 186: 361-366.Kemper et a/. (1998). Eur. J. Biochem., 253: 720-729.Kim, W.S. (1991). Res. Reports of the Rural Development Administration, Hort., 33: 16-26.Kitamura, H. and Yoneyama, T. (1994). Japanese J. Soil Sci. Plant Nutr., 65: 660-669.Kodde, K. etaJ. (1991). Fruitteelt(Den Haag), 81: 19.Kreij, C.DE (1990). Groenten en Fruit, 46: 35.Krelj, C.DE (1992). J. Hort. Sci., 67: 45-50.Kreij, C.DE (1996). J. Pl. Nutr. 19: 361-377.Lakshmi, B.S. et aI. (1997). Ann. Agric. Res., 18: 184-187.Leland, W. Lee et aJ. (1990). J. PI. Nutr., 13: 187-200.Leonard, RT. and Hepler, PK (1990). Rockville, Maryland, U.S.A; American Society for Plant Physiologists XV +

205 pp.Levchenko, V. et aJ. (2005). PNAS, 102: 4203-4208.Uu HUi Chao and Han Zhen Hai (1997). J. Fruit Sci., 14: 73-78.Lopez, MV. and Satti, 5.M.E. (1996). Plant Sci. (Limerick), 114: 19-27.Lou, 5.5. and Chen, YX (1990). Plant Physio!. Commun. No.1, 44-46.Maffei et al. (2004). Plant Physiol., 134: 1752-1762.Maksoud, M.A. eta/. (1995). Ann. Agric. Sci. (Cairo), 40: 771-780.Marcelis, L.F.M. et aI. (1999). J. Exp. Bot., 50: 357-363.Marschner, H. (1986). Mineral Nutr. Higher Plants. Academic Press, New York, NY.Montag, J. et aI. (2005). Intel conference on biological and pro-ecological methods for control of diseases in

orchards and small fruit plantations, Aug 29-31, 2005, Skierniewice, Poland.Montoro, P. eta/. (1995). J. Exp. Bot., 46: 255-261.Moon Byung Woo et a/. (1998). J. Korean Soc. Hart. Sci., 39: 454-459.Moon Byung Woo et a/. (1998). J. Korean Soc. Hort. Sci., 39: 716-720.Nagy, 5. eta/. (1985). J. Hort. Sci., 60: 137-140.Nachtigall, G.R. et a/. (1998). Revista Brasileira de Fruticultura, 20: 158-166.Navarro, J.M. et a/. (1999). J. Hort. Sci. Biotech., 74: 573-578.NG. K.Y. Carl and Mcanish. R. Martin (2003). Ann. Bot., 92: 477-485.

244 AGRICULTURAL REVIEWS

Olivwia, M.S.DE et al. (1995). Ecossistema., 20: 177-181.Olsen, WW. eta!. (1997). Gartenbauwissenschaft., 62: 61-65.Oosthuyse, SA (1997) Year book- South African Mango Growers' Association, 17: 29-32.Paiva, EAS. et al. (1998). J. Pl. Nutr., 21: 2653-2661.Paiva, EAS. et al. (1998). J. PI. Nutr., 21: 26.63-2670.Pascual, B. et al. (1996). Acta. Hort., 407: 327-332.Perring, M.A. and Pei'lrson, K (1987). J. Hort. Sci., 62: 303-304.Plese, L.P.M. et al. (1998). Sci. Agricola., 55: 144-148.Plisek, B.(1995). Acta. Hort., 383: 463-474.Raese, J.T. et al. (1995). J. Pl. Nutr., 18: 823-838.Raese, J.T. et al. (1996). J. Pl. Nutr., 19: 1131-1155.Raese, J.T. (1999). Good Fruit Grower, 50: 32-33.Raese, J.T. (1991). Good Fruit Grower, 42: 25-27.Randall, D.o. and Blevins, D.G. (1990). Current"Topics in Plant Biochem Physiol9, XII + 442 pp.Rersting, F. (1998). Die Bedeutung des kalziums fur die hohere Pflanze. Des Forschungsdienst., 5: 48-57.Resnizky, D. et al. (1991). Alon Hanotea, 45: 939-949.Safdar, S.S.H. eta1. (2001). Pak. J. BioI. Sci., 4(6): 707-710.Salinas, R. et al. (1986). J. Hort. Sci., 61: 343-347.Sarti, S.M.E. et al. (1995). Commun. Soil Sci. Plant Analy., 26: 2749-2760.Saha, D.P. et al. (1998). Agric. Rev., 19: 257~263.--Schroeder, J.t and Thuleau, P. (1991). Plant Cell., 3: 555-559.Schubert, E. et al. (1990). Agron.J., 82: 969-972.Sekse, L. (1998). Acta. Hort., 468: 637-648.SiddiquI. S. and Bangerth. F. (1995). J. Hort. Sci., 70: 949-953.Siddiqui. S. and Bangerth. F. (1995). J. Hort. Sci., 70: 263·269.Siddiqui. S. and Bangerth. F. (1996). J. Hort. Sci., 71: 703-708.Silva et al. (1997). Revista Fruticola, 18: 15-18.Spiers, J.M. (1993). J. Plant Nutr., 16: 2333-2339.Stow, J. (1993). Postharvest BioI. Technol., 3: 1-9.Strydom, G,J. et al.(1999). Deciduous Fruit Grower, 49: 51-56.Sugar, D. etat. (1992). Hort-Technol., 2: 382-387.SunDong Whan (1998); RDA J. Hort. Sci., 40:55-60.Svenson, S.E: and Witte, WT. (1992). J. Environ. Hort., 10: 125-129.Tahtiharju et al. (1997). Planta, 203: 442-447.Tahtiharju et al. (2001). Plant J., 26: 461-470.Taylor, M.A. et al. (1993). Sci. Hort., 54: 131-141.Tirlapur, UK et a1. (1992). Sexual Plant Reproduction, 5: 214-223.Tomala, K. (1997). Acti'l Hort., 448: 59-65.Toselli, M. et al. (1998). Rivista di Frutt/coltura e di Ortoflorlcoltura, 60: 45-48.Treshow, M. (1970). Environment.and Plant Response. McGraw Hill Book Co., NY.Tretvn, A. et a!. (1994). J. Plant Physlol., '144: 562-568:Tu, S.1. etal. (1992). Plant and Cell PhysiOI., 33: 519-525.Tzoutzoukou and Bouranis (1997). J. Plant Nutr., 20: 295-309.Vaysse, P. et al. (2001). lnfos-CtIfl., 170: 30-33.Vranova, E. et al. (2001). J. Exp. Bot., 52: 181-182.Wada, T. and Ikeda et al. (1996). J.Japanese Soc. Hort. Sci., 65: 553-558.Wertheim, S.J. et al. (1995). Fruitteelt(Den Haag), 85: 20-21.Witney, G.w. etal. (1991). Sci.Hort., 47~173-176.WuI, M. and Takano;T. (1995). EnViron. Control BioI., 33: 7-14.White, J. Philip et al. (2003). Ann. Bot., 92: 487-511, 2003.Xiao Yan et al. (1998). China fruits, 24: 25-28.Xu, Haixin and Heath, Michele (1998). Plant Cell, 10: 585-598.Younis, M.E. et al. (1994). Egyptian J."'"PhYSiol. Sci.•,IS: 393-406.Zaragoza, S. et a1. (1996). J. Hort. Sci., 71,: 32'~.p't6.Zindler-Frank, E. (1995). Botanica Ag.t~.r·l~ 144-148.Zindler-Frank, E. (1991). Botanica Acta., 104: 229-232.Zocchi,G. et al. (1995). Acta. Hort., 383: 15-23.Zora Singh et al. (1991). Plant and SOil, 133: 9-15.

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Appendix Iwww.aIDYine.adelaide.edu.auwww.ars.usda.govwww.iistrabiology.arc.nasa.gov .www.blo21.bas.bgwww.bioone.orgWWW.biol.uni.torun.plwww.biozentium.uni-urierzburg.dewww.cplpress.comwww.danforthcenter.orgwww.deccanherald.comwww.dynaweb.oac.edIib.org:8088/www.facultyofl000.comwww.fiu,eduwww.garfield.library.upenu.eduwww.hesi.nlwww,hort,iastate.eduwww.icmb.ed.ac.ukwww.indstate,eduwww.ingentacopnect.com!contentlurbanI271www.jxb.oupjournals.orgwww.ncbi,nlm,nin,gQvwww.plantscience.acpfg.com.auwww.plantcell.org/cgilcontent/abstract/3/4/333WWW.plantsci.com.ac.ukwww.pirl.f;lduwww.plantphys.netwww,plantphys,wsu,eduwww.sciencf;l.uva.nlwww.sciencedirect.comwww.spacebio.netwww.ssoar.org/research/plant-physio.htmwww.tard.state.tx.uswww.technion.ac.ilwww.trap.kvI.dkwww.trna,chem.yalf;l.eduwww.unjge.chwww.uta.eduwww.vrg.orgwww.zbm.uni-kif;ll.

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A BRIEF SUMMARY OF THE EFFECT OF CALCIUM IN REGULATINGTHE FUNCTIONG OF THE PLANT SYSTEM

1. Effect on the structural component of plant tissues• Regulating cell wall construction• Streaming of cytoplasmic organelles• Spindle fibre formation

2. Direct influence upon plant development by Ca would include• pH alteration• Enzyme activation• Ion balance• Membrane permeability• Ion uptake• Water transpiration.

3. Indirect or edaphic effect of Ca• Soil formation• Humification• Nutrient accumulation• Neutralization of acids

4. Endogenous characteristics of Ca within higher plants• Low ionic activity within the cell cytoplasm• Low physiological mobUity through the plant• Mediation in many different processes

5. Control of several plants diseases• Fruit cracking• Blossom end rot• Peel pitting and bitter pit• Bract distortion and bract necrosis• Browning and Black patch• Skin bursting, side rot and tip burn

6. Preharvest treatment reduce postharvest losses by increase in Vit C• Firmer fruits• Increases Vit C• Reduces severity of postharvest fungal decay• Production of new membrane protein• Better appearance of products

7. Physiological effects of calcium• Induces additional cell division in bundle sheath extensions• Free calcium ions stimulate flowering• Enhances reducing sugar content and growth in plants• Serves as a second messanger• Lower activity of polygalacturonase during storage• Recovery from freeze injury• Prevents plants against drought and salinity conditions.