ISSN 1392-3196 ŽEMDIRBYSTĖ=AGRICULTURE Vol.99,No.2(2012) 111

ISSN 1392-3196 Žemdirbystė=Agriculture,vol.99,No.2(2012),p.111‒124UDK634.1:581.17:576.3

Chilling injury in chilling-sensitive plants: a review

AlexanderS.LUKATKIN1,AušraBRAZAITYTĖ2,ČeslovasBOBINAS2,PavelasDUCHOVSKIS2

1MordovianStateUniversityBolshevistskaja68,Saransk,RussiaE-mail:aslukatkin@yandex.ru2InstituteofHorticulture,LithuanianResearchCentreforAgricultureandForestryKauno30,Babtai,Kaunasdistr.,LithuaniaE-mail:p.duchovskis@lsdi.lt

AbstractChilling temperatures (1–10ºC) lead to numerous physiological disturbances in the cells of chilling-sensitiveplantsandresultinchillinginjuryanddeathoftropicalandsubtropicalplants,e.g.,manyvegetablespecies.Theliteraturereviewshowsthattheexposureofchilling-sensitiveplantstolowtemperaturescausesdisturbancesinallphysiologicalprocesses–waterregime,mineralnutrition,photosynthesis,respirationandmetabolism.Inactivationofmetabolism,observedat chillingof chilling-sensitiveplants is a complex functionofboth temperature anddurationofexposure.Responseofplantstolowtemperatureexposureisassociatedwithachangeintherateofgenetranscriptionofanumberoflowmolecularweightproteins.Thereviewanalyzeshistoricalaspectsinthedevelopmentofideasaboutthenatureofchillingdamageofchilling-sensitiveplantsanddirectionofmodernresearch.Basedontheauthors’ownresearchandtheliteraturedata,theconceptofcolddamagewasproposed,whichhighlightedtheleadingroleofoxidativestressintheinductionofstressresponse.Accordingtothisconceptthereweredistinguishedpossiblewayshowtoimprovecoldtolerance.They were divided into several groups: the thermal effect (low-temperature hardening, thermal conditioning,intermediatewarmingandtheeffectofheatstress),chemicaltreatment(traceelements,syntheticgrowthregulators,antioxidants)andtheuseofgeneandcellengineering.

Keywords:antioxidants,cell,chilling-sensitiveplants,chillinginjury,physiologicalprocesses,oxidativestress.

IntroductionMore than half of the 350 000 plant species

onEartharegrowninthetropicsandsubtropics.Inthecourseofevolution,theycouldnotdeveloptheabilitytowithstandlowtemperatures(Лукаткин,2002).Mostofthesespeciesaredamagedduringstorageattemperaturesabovethefreezingpointoftissues,butlowerthan15°C(chilling temperatures). This damage is called chillinginjury as opposed to damage during freezing (freezinginjury)(Levitt,1980;Raison,Lyons,1986).Thus,chill-ing injury is damage to chilling-sensitive plant speciesduringstorageat temperaturesabovethefreezingpointoftissues,butlowerthan15°C.Chilling-sensitive plants aretheplantssensitivetochillinganddamagedatchill-ingtemperatures.

Theabilityofplantsinavegetativestatetosur-vivetheactionofchillingtemperatureswithoutharmtothefuturegrowthanddevelopmentiscalledcoldresist-ance(Генкель,Кушниренко,1966;Коровин,1969).Inturn, chilling-sensitive plants are sensitive to chillingandafterprolongedstorageinthesetemperaturesexter-nalsymptomsof injuryaredevelopedanddeathof the

organismoccurs (Table).Plants,whichhave thevisualinjuries at temperatures above 15°C, are called “verysensitive to chilling” (Raison,Lyons, 1986).Anumberoftropicalorsubtropicalplants,suchasrice,maize,to-mato,cucumber,cotton,soybeans,etc.,introducedinthehigherlatitudeshavenotacquiredsubstantialresistancetochilling,despitethelonghistoryofcultivationintem-perateregions(Wilson,1985).

Chilling temperatureseffectsonplants in tem-perateclimatesleadtoareductionorcompletecropfailureduetoeitherdirectdamageordelayedmaturation.Evenasmalldropintemperature,causingnovisibledamagetochilling-sensitiveplants,causedtoupto50%reductionintheirproductivity(Коровин,1969).Forexample,chillingdamage toyoungcottonplants inU.S. in1980resultedinthelossof60milliondollars.InSouthandSouth-EastAsia,high-yieldingvarietiesofricearenotgrowninareasofmorethan7millionhectares,wheretheymaybeex-posedtochillingtemperatures(Wilson,1985).Obviously,theproblemofplantresistancetochillingtemperatures,whichoftenoccurinspringandautumninmanycount-ries,isimportantforpracticalplantbreeding.

112 Chilling injury in chilling-sensitive plants: a review

Themostnoticeablevisualsymptomsofchill-ing injury in herbaceous plants are leaf and hypocotylwilting (Mitchell,Madore, 1992;Frenkel,Erez, 1996),whichoftenprecedestheappearanceofinfiltration(wa-tersaturatedareas)(McMahonetal.,1994;Sharometal.,1994), theappearanceofsurfacepitsandlargecavities(Dodds, Ludford, 1990; Cabrera et al., 1992; Frenkel,Erez,1996),discolorationofleavesandinternaltissues(Sharometal.,1994;Yoshidaetal.,1996;Tsudaetal.,2003), acceleratedagingand ruptureof chilled tissues,slow, incomplete or uneven ripening (Dodds, Ludford,1990), accompanied by a deterioration of the structureandflavor (Harker,Maindonald,1994;Ventura,Mend-linger,1999);increasedsusceptibilitytodecay(Cabreraet al., 1992),dryingof the edgesor tipsof leafblades(Жолкевич,1955;Hahn,Walbot,1989)andinthecaseof prolonged chilling – leaf necrosis and plant death(Mitchell,Madore,1992;Capell,Dörffling,1993;Fren-kel, Erez, 1996).According to Skog (1998), potentialsymptomsof chilling injury are surface lesions,water-soakingoftissues,waterloss,desiccationorshrivelling,internaldiscolouration,tissuebreakdown,failureoffruittoripen,orunevenorslowripening,acceleratedsenes-cenceandethyleneproduction,shortenedstorageorshelflife,compositionalchanges,lossofgrowthorsproutingcapability, wilting and increased decay due to leakageofplantmetabolites,whichencouragegrowthofmicro-organisms,especiallyfungi.

Seeds of chilling-sensitive plants do not ger-minate at temperatures below 10–15°C (Wolk,Herner,1982;Ismailetal.,1997),andbythisparametercanbedivided into twomaingroups (Markowski, 1988).Theseedsofthefirstgroup(representatives–Solanaceaeandpumpkin) are not damaged during imbibitions at chill-ing temperatures.With temperature increase theygrownormally,butinitiationofrootgrowthleadstounderde-velopedroottiptissue,tissuenecrosisaftertheroottip,damagetothecortexorstele(Bradow,1990;Jennings,Saltveit,1994).Thesecondgroupincludesplantswhoseseedsareparticularlysensitivetolowtemperaturesduringimbibitionsandmaynotgerminateatlowtemperatures:beans, soybeans, chickpeas, corn, and cotton (Gorecki

et al.,1990;Zemetra,Cuany,1991).There,plantdamageisincreasedbysoilpathogens,althoughitisasecondaryfactor(Wolk,Herner,1982).

Acharacteristiceffectofchilling temperatureson chilling-sensitive plants is growth slowing, morepronouncedinsusceptiblespeciesandvarietiesincom-parisonwiththetolerantspecies(Tingetal.,1991;Rab,Saltveit,1996a;Venemaetal.,1999).Inaddition,thereisadelayeddevelopmentandlengtheningofthegrow-ing season (Skrudlik, Koscielniak, 1996).At the sametimeapicalconedifferentiationisdelayed,reducingthenumber of newly formed plant organs and the rate oftheir occurrence, the structureof roots is changed, andflowering rate, fruit and seed filling are reduced (Buisetal.,1988,Barlow,Adam,1989;Rab,Saltveit,1996b,Skrudlik,Koscielniak,1996;Lejeune,Bernier,1996).

Cytophysiological changes caused by chilling in the chilling-sensitive plants Chilling temperatures cause multiple disor-

ganizationsofthecellsultrastructureinsensitiveplants(Kratsch,Wise,2000).Thedamagingeffectofchillingisoftenrevealedinthedestructionofthecellsmembranesystems, leading to lossofcell compartmentation (Gu-tierrezetal.,1992).Itwasshowntheswellingandrup-tureoftheplasmalemma(Taoetal.,1991),destructionoftheendoplasmicreticulumandvesiculationofitsmem-branes(Marangonietal.,1990),andchangesoftheGolgiapparatus(Yoshidaetal.,1989).Uponchilling,themostnoticeablechangeswereshowninthestructureofmito-chondria,namelytheirswellinganddegeneration(Guti-errezetal.,1992),matrixenlightenment,cristaeshorten-ingandadecreaseintheirnumber,whichshouldleadtoareducingofoxidativephosphorylation(Desantisetal.,1999;Yinetal.,2009).Chillingtemperaturesdisturbedthe formation of prolamellar plastids (Ikeda, Toyama,1987), caused swelling and structural changes in chlo-roplasts,namelydestructionofchloroplastsmembranes,disintegrationofgrains,reductionofribosomenumber,

Table.Thelistofthevegetables,sensitivetochillingtemperatures,thelowestsafestorage/handlingtemperatureandthesymptomsofchillinginjury(DeEll,2004)

Crop LowestsafetemperatureºC Chillinginjurysymptoms

Asparagus 0–2 dull,gray-green,limptipsBean(snap) 7 pittingandrussetingCucumber 7 pitting,water-soakedlesions,decayEggplant 7 surfacescald,Alternariarot,seedblackeningOkra 7 discoloration,water-soakedareas,pitting,decayPepper 7 pitting,Alternariarot,seedblackeningPotato 2 mahoganybrowning,sweeteningPumpkin 10 decay,especiallyAlternariarotSquash 10 decay,especiallyAlternariarot

Sweetpotato 10 decay,pitting,internaldiscolorationTomato(ripe) 7–10 water-soaking,softening,decay

Tomato(mature-green) 13 poorcolourwhenripe,Alternariarot

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inducedtheformationofperipheralreticulum(smallve-siclesofenvelope)andtheaccumulationoflipidbodies,andthedisappearanceofstarchgrains(Gutierrezetal.,1992;Kratsch,Wise,2000).

The sharp decrease in the number of divid-ingcellsduringchillingdecreased themitotic index inapexesandinthebasalpartofyoungleaves(Зауралов,1993;Лукаткинидр.,2010).Therelationshipbetweenthecellcyclephaseswaschangedtoo(Francis,Barlow,1988;Rymenetal.,2007).Significantreductionofcellgrowth inrootelongationzoneat lowtemperaturewasshown (Ikeda et al., 1999). Chilling temperatures causeaccelerated cell differentiation. So, in chilled root apex-esofmaizetheprogressingdifferentiationofsomecelllineswasobserved(Zavala,Lin,1989).Inhibitionofcellgrowthleadstosignificantchangesingrowthoftheplantanditsorgans(Rab,Saltveit,1996a;Rymenetal.,2007;Straussetal.,2007).

Colloid-chemicalpropertiesofthecytoplasmareaffected by chilling too (Генкель, Кушниренко, 1966;Wang, 1982; Minorski, 1985). So, cytoplasm viscositydecreasesataslightchillingdue to the increaseofcol-loids dispersion anddecayof structural formations, butitgrowsatastrongandlong-termchillingduetocoagu-lationofstructuralproteins (Жолкевич,1955;Генкель,Кушниренко,1966;Zhangetal.,1995).Thecontentofsolubleproteinswasdecreasedinchilling-sensitiveplantsat low temperatures, and this led to a reduction in theisoelectriczoneofthecytoplasm(Дроздовидр.,1977).ChillingofsensitiveplantsleadstoashiftofintracellularpH(Yoshida,1994;Zauralovetal.,1997;Kasamoet al.,2000) and an increase in cell membranes permeability(Markowskietal.,1990;Lukatkinetal.,1993,Лукаткини др., 2007).A very sensitive indicator of the cell is acytoplasmic streaming, which was stopped for severalminutesafterchillingofsensitiveplants(tomato,tobacco,andpumpkin)to10°C(Lewis,1961).Otherstudiesfoundagradualdecelerationofthecytoplasmicstreaminginthetrichomesoftomato,watermelon,spiderwortanddigitaliswhenthetemperaturedroppedbelow5°C(Pattersonetal.,1979),andthestreamingratecorrelatedwithresistanceofplantstochillingtemperature.Thechangesincyclosisre-sponsetochillingwereassociatedwithchangesinthecy-toplasmviscosity,ATP(adenosine-5’-triphosphate)level,sensitivitytochillingofenzymesystemsresponsiblefortheuseofATPfor thestreaming,withdamagingof thecytoskeleton(Pattersonetal.,1979;Wang,1982;Woodsetal.,1984b;Minorsky,1985).

Effect of chilling on the physio-logical processes in chilling-sensi-tive plants Incubation of chilling-sensitive plants at low

temperaturesinducesdisturbancesinphysiologicalpro-cesses: water regime, mineral nutrition, photosynthe-sis, respirationand totalmetabolism(Жолкевич,1955;Генкель,Кушниренко,1966;Levitt,1980;Wang,1982;Graham,Patterson,1982).

Water regime. Chilling of sensitive plants af-fectsallcomponentsofwaterregimeandcauseslossof

water, resulting instrongwilting (Vernierietal.,1991;Boeseetal.,1997;Bloometal.,2004).Itisbasedonthetwomainfactors:rapiddeclineintheabilityofrootstoabsorbwaterandtransportittotheshoots(Bolgeretal.,1992)andreducedabilitytoclosestomatainresponsetosubsequentwaterdeficit(Pardossietal.,1992;Wilkinsonetal.,2001;Bloometal.,2004).Insufficientwatersup-plyprovokesrapiddropinwaterpotentialofleavesdur-ingthefirsthoursofcooling(Wolfe,1991;Capell,Dörf-fling,1993;Boeseet al.,1997).Thedegreeofchillingdamageofplantscanbereducedbymeansofpreventingthedisturbanceofthewaterregime(Vernierietal.,1991;Wolfe,1991;Pardossietal.,1992;Janowiak,Dörffling,1996;Boeseetal.,1997).

Mineral nutrition. Low temperatures have aneffectonmineralnutritionofplants.Absorptionofionsbyrootsisdifficult,aswellastheirmovementintheabove-ground parts of plants.The distribution of nutrients be-tweentheplantorgansisdisrupted,withgeneraldecreasein the nutrient content in the plant (Лукаткин, 2002).Chillingofplantsleadstoadecreaseintheactivityofnit-ratereductase,reductioninthenitrogenincorporationintheaminoacidsandproteins,andadropintheproportionoforganicphosphorusandanincreaseininorganicPcon-tent(Holobradaetal.,1981;Ziaetal.,1994),whichisaconsequenceofabreachofphosphorylationandenhanceddecompositionoforganicPcompounds.Mechanisms toreducetheabsorptionofnutrientsbychillingtemperaturesinclude depression of respiration and/or oxidative phos-phorylation, impair enzymatic transport systems associ-atedwithconformationalproteinschangesinmembranes,changes in membrane potential, reducing the supply ofATP toH+-transportingATPase, aswell as lowering thepermeabilitycoefficientsforions(Clarksonetal.,1988).

Respiratory rate. The consequence of keepingplants at chilling temperatures is a change in respira-tory rate.There is evidence of its decline, occurring asaresultofdestructionofthemitochondriastructure,thegeneralloweringofkineticenergy,andtheinhibitionofsomeenzymes(Lyonsetal.,1979;Yoshidaetal.,1989;Prasadetal.,1994a;Lawrence,Holaday,2000;Munroet al.,2004).Otherauthorshaveobservedthatanincreaseinrespiratoryactivityduringchillingandprolongedele-vation of the respiration rate after cold exposure mayindicateirreversiblemetabolicdysfunctionandaccumu-lation of incompletely oxidized intermediates (Wilson,1978; Steward et al., 1990;Yadegari et al., 2008).Themechanismofstimulationisunknown,butitispossibletoassumethatitwastheresultofuncouplingofoxidativephosphorylation(Wang,1982).Itisalsopossiblethattheincreasedrespirationreflectsareactiontothetransferofplantsfromchillingtemperaturestothehighertempera-tures(Zauralov,Lukatkin,1997).Asaresultofdecreasedrespiration and increased consumption of energy-richphosphatesatchillingtemperaturesisareductionofATPlevels (Takeda et al., 1995; Lawrence,Holaday, 2000).Cold-tolerant crop species have greater temperaturehomeostasisofleafrespirationthancold-sensitivespecies(Yamori et al., 2009). Chilling reduces the cytochromepathoftheelectrontransportinseedlings(Prasadetal.,

114 Chilling injury in chilling-sensitive plants: a review

1994a;Reyes,Jennings,1997)andenhancesalternativerespiratory pathways (Ordentlich et al., 1991; Purvis,Shewfeld,1993;Gonzalez-Meieretal.,1999;Ribascarboetal.,2000).Perhapsthesealternativepathwaysplayanimportant role in plant adaptation to chilling (Stewardet al.,1990).Theyaretriggeredatthechillingperiodandincreasewith decreasing temperature (Ordentlich et al.,1991). These alternative pathways induced by chillingcausedadecreaseinsuperoxidegeneratedinmitochon-dria(Purvis,Shewfelt,1993;Huetal.,2008).

Rate of photosynthesis.Duringandafterchill-ing,therateofphotosynthesisintheleavesofchilling-sensitive plants decreased and this is more related todecreasing temperature and lengthening of chilling pe-riodandpersistedforalongtimeaftertransferofchilledplantsintheheat(Jandaetal.,1994;Boeseetal.,1997;Sonoike,1998;Gesch,Heilman,1999;Allen,Ort,2001;VanHeerdenetal.,2003;Lietal.,2004;Straussetal.,2007).Thephysiologicalreasonsforthesuppressionofphotosynthesisaretheinhibitionofphloemtransportofcarbohydrates from the leaves, stomatal limitation, de-structionofthephotosyntheticapparatus,damagetowa-ter-splitting complex of photosystem I, inhibiting elec-tron transport, and uncoupling of electron transfer andenergystorage,changesintheactivityandinhibitionofsynthesisofkeyenzymesoftheCalvincycleandC4-way(Yordanov,1992;Nieetal.,1992;McMahonetal.,1994;Gesch,Heilman,1996;Yoshidaetal.,1996;Terashimaetal.,1998;Kingston-Smithetal.,1999;Venemaetal.,1999;VanHeerden et al., 2003;Garstka et al., 2007).Cold-sensitive crop species have smaller temperaturehomeostasis of leaf photosynthesis than cold-tolerantspecies(Yamorietal.,2009).

Chilling of sensitive plants in light hadmuchstrongereffectsonthephotosyntheticapparatusthanchill-inginthedark(Szalaietal.,1997;Alam,Jacob,2002).Itisconsideredthatadisturbanceofphotosynthesisduetothelightchillingislargelyaresultofphotoinhibitionand photooxidation occurring in the chilling-sensitiveplants (butnot cold-resistant), asa resultof theexcessenergy of excitation obtained by photosynthetic appa-ratus.Photoinhibitionofphotosynthesis is theloweringof photosynthetic activity under excessive illuminationduring chilling (Nie et al., 1992;Wang et al., 2008 a).It increaseswithdecreasingtemperatureandincreasinglightintensity(Jandaetal.,1994;Greer,1995).Primarysite photoinhibition is the photosystem II. However, itwasdiscoveredthatphotoinhibitionoccursatrelativelylowlightandlowtemperature,andthemainsiteofdam-ageisphotosystemI(Sonoike,1996;1999).Decreaseofphotosynthesisatchillingtemperaturesmaybeaconse-quenceofphotooxidativedamagetothephotosystemsinthemembranesofchloroplasts,which ismanifestedbyincreasedlipidperoxidation,degradationofchlorophyll,carotene,andxanthophylls(Fryeretal.,1998;Kingston-Smith,Foyer,2000).Itwascausedbyactivatedoxygenspeciesandwasassociatedwithreducedantioxidantac-tivityof tissues (Leipner et al., 1997;Terashimaet al.,1998;Leipneretal.,2000;Alam,Jacob,2002).

The inactivation of metabolism is a complexfunction of both temperature value and duration of its

effects(Breidenbachetal.,1990).Itisdifficulttodistin-guishbetweenmetabolic changes in chilledplants, oc-curringasaresultofchillingdamageorprecedingit. So,protein content in tissues of chilling-sensitive plants isusuallyreducedwithchilling,mainlyduetoasharpde-creaseinsynthesis(Levitt,1980;Mercadoetal.,1997).Asaresultofinhibitionofproteinsynthesisistheincreaseintheleveloffreeaminoacids(Kanda,1998),especiallyproline(Duncan,Widholm,1991;Jouveetal.,1993),ac-cumulationofwhichisconsideredastheelementofthemechanismofcoldhardening.Lowtemperaturesreducetheactivityofmanyenzymes(Guy,1990).Thereasonsforthismaybethedissociationofmultimericenzymes,protein-lipidandhydrophobicinteractionsdisorders,re-versible changes in kinetic properties of enzymes andallosteric regulation (Graham,Patterson, 1982;Matsuoet al.,1994).Keepingthechilling-sensitiveplantsatlowtemperaturetheconcentrationofsolublesugarsincreasedand starch contentdecreased significantly in all organs(Jouve et al., 1993). Changes in the level of carbohy-dratescausedbythechillingareassociatedwithimpairedrespiration,photosynthesis,andtheactivityofenzymesofcarbohydratemetabolism(Ebrahimetal.,1998).

Variousphysiologicalfunctionsarenotequallysensitivetocooling(Wilson,1978;Yoshidaetal.,1989).Physiologicaldysfunctioninducedbylowtemperatures,can be converted (or function restored) if the tissue isreturned to normal temperature before the appearanceofdamage.Thus,temperaturesbelowcriticaltriggerthedisturbancesofphysiologicalfunctions,butthesedistur-bancesdonotleadtovisiblemanifestationsofinjuryortochangesintherateofgrowthanddevelopment,sincedisturbancesofthephysiologicalprocessesarereversibleuntiltheybecomestable(Lyonsetal.,1979).Irreversibledamagearisingfromprolongedchillingmaybecausedbytheaccumulationoftoxicmetabolites(Lyons,1973;Graham,Patterson,1982).

Molecular-genetic changes During growth, plants are exposed to various

abiotic stresses such as low temperature, salt, drought,flooding,heat,heavymetaltoxicity,etc.Plantsmustbeable to respond appropriately to the stress. In nature,manystressesaffectplantstogether.Duetothecomplexnatureof stress,multiple sensors aremore likely toberesponsibleforperceptionofthestress.Aftertheinitialrecognition of the stress, a signal transduction cascadeisinvoked.Secondarymessengersrelaythesignal,ulti-matelyactivatingstress-responsivegenesgeneratingtheinitialstressresponse(Mahajan,Tuteja,2005;Grennan,2006;Duchovskisetal.,2006;Oktemetal.,2008).NowitisknownthatdroughtandsaltstresseswerefoundtoinducemanyofthesamegenesasdiddroughtstressandABA application or response to both cold and salinitystresses is regulatedbygenesofcalcium-signalingandnucleicacidpathways(Mahajan,Tuteja,2005;Grennan,2006).Apparently,thatchillingsensitivityisgenericallydetermined, and the species and varietal differences ofchillingresistanceareconnectedtodefinitegenes(Pra-sadetal.,1994a;Sabehatetal.,1998;Grennan,2006;Suetal.,2010).Therewereidentified634chilling-respon-

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sivegenesinthechilling-lethalmutantsofArabidopsis.Thisgenelistincludesgenesrelatedtolipidmetabolism,chloroplastfunction,carbohydratemetabolism,freeradi-caldetoxification(Provartetal.,2003).Insweetpotatothere were examined transcriptional regulation of ex-pansingenesinresponsetovariouschillingtemperatures(Nohetal.,2009).90%ofthe108cDNAclonesoflowtemperature-grownsunflowerplantsexpressedatvarioustemperaturesweretobedown-regulatedandinvolvedinthemetabolismof carbohydrate, protein synthesis, sig-nal transduction and transport function (Hewezi et al.,2006).Responseofplantstolowtemperatureisassoci-atedwith a change in the rate of gene transcription oflow molecular weight proteins. Even very brief plantexposures to chilling temperature are sufficient for theappearanceof stressproteins.Cooling several chilling-sensitive plants (corn, rice,waving, tomato, cucumber,peanuts,cotton,sunflower,etc.)inducedthesynthesisofmorethan20polypeptideswithmolecularmassesof14to94kDa,whichweresimilartoHSP,inducedbyhea-ting,ordifferentfromthem(Hahn,Walbot,1989;Pareeketal.,1997;Lietal.,1999).Coldacclimationofchilling-sensitive plants is also accompaniedby the changes insynthesisofseveralproteins(Hahn,Walbot,1989;Guy,1990;Cabaneetal.,1993;Andersonetal.,1994).Chill-ingleadstodifferentialexpression(down-regulatedandup-regulated)ofgenesencodingdifferentproteins(VanHeerdenetal.,2003;Yamagitchi-Shinozaki,Shinozaki,2006;Rymenet al.,2007;Wangetal.,2008a).

Cell membrane changes Low temperaturesalter thephysicalproperties

ofcellmembranes.Chillingofsensitiveplantsleadstomultiplechangesintheirmembranes,namelyreducethemembrane elasticity, decreasing their compliance andpreventing lipid inclusion in their composition, lowerlipid fluidity, thereby reducing the activity of severalmembrane-bound enzymes, including H+-ATPase, in-creasethelateraldiffusionofphospholipids,sterolsandproteinsintheplasmamembrane(Quinn,1988;Kasamoet al., 1992;Koster et al., 1994;Kasamoet al., 2000).Thephasetransitionofcellmembranesoccursatchillingtemperaturesinchilling-sensitiveplants(butnotcold-re-sistant),andmembranesfromflexibleliquid-crystalturnintosolid-gelstructure,leadingtochangesintheproper-tiesofmembranesandmembrane-boundenzymeactivity(Raisonetal.,1971;Lyons,1973).Itisbelievedthatthephase transitions of even small fractions ofmembranelipidsresultintheformationofsoliddomainsthatcausecellmembraneandcelldamage(Thompson,1989).Thephaseseparationofthemembranecomponentsislinkedwithphasetransition.Thisphaseseparationischaracter-izedbytheappearanceofgel-likesitesintheplaneofthebilayerlipid.Thesesitesarepartiallyorcompletelyfreeofproteins.Whenthecellswerenotdamaged,theforma-tionof thesemicrodomainswasofa temporarynature.The disturbances became irreversible with long-termchilling, and coincided with the appearance of visualsymptoms of damage (Platt-Aloia, Thomson, 1987).Anumberofspeciesoftropicaloriginhavethelateralphase

separationtemperaturesomehigher(15°C)thaninplantsfromtemperatezones(6–8°C)suggestingthatplantsre-ducethefreezingpointofmembraneswiththedistancefromzoneoftropicalorigin(Terzaghietal.,1989).

Thelipidcomponentsofmembranesareconside-redthemostimportantforthemembranesfunctioningatlowtemperatures(Lyons,1973;Lyonsetal.,1979;Nish-ida,Murata, 1996; Routaboul et al., 2000). Chilling ofsensitiveplantscausesdegradationofgalacto-andphos-pholipids,resultinginincreasedfreefattyacids.Chillingofplantsandfruitschangedthemolarratioofsterolsandincreased the ratio of sterols/phospholipids,whichmaybeonereasonforloweringthemembranefluiditywhencooled (Wang et al., 1992; Whitaker, 1993). Chilling-sensitiveplantsgrowingatlowerhardeningtemperatureshowanincreaseinunsaturatedfattyacids,phospholipidsaccumulation in the tissues, lower levels of sterols andtheiresters,whichreducedtheratioofsterol/PL(Kasamoetal.,1992;Kojimaetal.,1998;Kaniugaetal.,1999).

Exposureofchilling-sensitiveplantstolowtem-peraturechangesproteincomponentsintheirmembranes.Thesechangesinclude:disordersofproteinstructure,thereleaseofnon-proteincomponentsofenzymes,changesinallostericcontrolofactivityandkineticparameters.Atthesametimetheprotein-lipidinteractionsinthemem-branehaveasignificantroleinthelow-temperatureinac-tivationofenzymes(Graham,Patterson,1982).

Changesinthestateofmembranesmayleadtosecondary or irreversible reactions, depending on tem-perature,exposuredurationandsensitivityofthespecies.Afteraprolongedchilling,thesechangeswillcauselossofmembraneintegrityandcompartmentation,theleakageofsolutes,decreaseofoxidativeactivityofmitochondria,increase of the activation energy of membrane-boundenzymes, reduce the rate of photosynthesis, cause dis-ruptionandimbalanceofmetabolism,theaccumulationoftoxicsubstancesandthesymptomsofchillinginjury(Lyons,1973;Levitt,1980;Quinn,1988).

The theory of chilling injury In the initial period of studying, the influence

of low temperatures on chilling-sensitive plants waswidespread theorySachs about thedeathofplantsduetodisordersofwaterregime.However,subsequentstud-ies have shown one-sided interpretation of these data.Changesinwaterregimewerelikelyduetodisturbancesof other processes. In themiddle of the 20th century itwasfoundthatthewiltingoftheaerialorgansisnotduetoexcessivetranspirationoverslowsupplyofwaterbyroots,butistheresultofloweringwater-holdingcapaci-tyduetodisorganizationofthecytoplasmstructureandmetabolicdecompensation(Жолкевич,1955).

Basedonobservationsofchangesinprotoplas-micviscosityatlowtemperatures,ithasbeensuggestedthat this cell property plays a key role in the damage(Belehradek,1935).Thelesstolerantplantstocold,thehighertemperatureatwhichcytoplasmgelingoccursandthe faster increases the viscosity of the cytoplasm.Atconsiderableincreaseinviscositytherateofbiochemicalreactionsinthecytoplasmisdecreased,themetabolism

116 Chilling injury in chilling-sensitive plants: a review

isdisturbed,whichleadstodysfunctionofphysiologicalprocesses.However,itwasshownthatcucumberplantsdecreasedviscositywithincreasingchillingduration,andtheworstafter2.5–4days,andthenincreasedgradually,reachingviscositylevelofnon-chilledplant,butshortlybefore the complete withering away could exceed thislevel.Anincreaseinviscosityofhighlydamagedplantsalso continued after the transfer into heat. “Dying” in-crease protoplasmic viscosity and is the final stage ofdeath,whichhasnorelationtothefirststageofdamage,butonlydeepensit(Жолкевич,1955).

According to data of some research from the1950–60s, the main result of chilling-sensitive plantsdamageduring long-termcooling is ametabolic disor-der. In this case, the death of plants occurs due to thepredominanceofthedestructionoverthesynthesis.Oneof theprobable causesof theprotoplasmstructuredis-organizationandirreversiblechangesinthemetabolismis the uncouplingbetween the energyobtainingduringrespiration and its effective consumption (Жолкевич,1955).However,metabolicchangesoccuronlyaftersuf-ficientlylongchillingofplantsandmostofthemaswellaschangesinwaterregimearenottheprimarycauseofchillinginjury.So,shorterdurationofchillingdoesnotcauseasharpinhibitionofmetabolism.Accumulationoftoxicproductsofmetabolismasaresultoftheimbalancethatoccursduringchillingofsensitiveplantsandisoneofthemainreasonsofchillinginjury(Жолкевич,1955,Генкель,Кушниренко,1966),whichoftenoccursafterthe return of chilled plants to heat, i.e. is the result ofsecondarydysfunctionassociatedwithheating.

Amongthehypothesesabouttheprimaryeventsthattriggertheoccurrenceofreactiontolowertempera-tures,hypothesisofphasechangeprevailedinthe1970s,according towhich thechilling-inducedchanges in themolecularorderingofmembranelipidsmaybethecauseof chilling injury (Raison et al., 1971).These changesincrease thedamagebyloweringtheATPlevels,meta-bolicimbalancesandincreasingmembranepermeability(Lyons,1973).However,allthesechangesdonotoccurimmediatelyafterthestartofchillingandarelikelytobesecondary disorders (Minorsky, 1985).The increase inmembranepermeabilityduetothelow-temperatureexpo-sure(“membranesleakage”)shouldbequick,registeredinthefirstfewminutesafterplacingthetissueatchillingtemperatures,inaccordancewiththehypothesisofphasetransitions.Inreality,thisdoesnothappen,andoftenpas-sivepermeabilityisnotincreased(Pattersonet al.,1979).Moreover,theincreaseinelectrolyteleakageislikelyduetochilling-inducedwaterstress,whichhasbeenrevealedto be considerably weaker in an atmosphere saturatedwithwater(Guinn,1971).Atthesametimeitisnotewor-thythatthelowunsaturationofmembranousphospholi-pides,whichisgenericallydetermined,givessensitivityto cold temperatures to chilling-sensitive plants (Zhuet al.,2008).Thedataabouttheintroductionofgenesoffatty acid desaturases in a genome of chilling-senitiveplantsconfirmsthatthisgivessensitiveplantsmorepro-nouncedchillingresistance(Kodamaet al.,1994;Ishiza-

ki-Nishizawaetal.,1996;Hamadaetal.,1998;Murata,Tasaka,1997;Domínguezetal.,2010).

Inrecentyears,specialattentionofresearchershasbeendrawntotwohypothesestoexplaintheinduc-tionofchillingdamagetoarapidincreaseintheconcen-trationoffreecytosolicCa2+([Ca2+]cyt)(Minorsky,1985)and theoccurrenceofoxidative stressuponchillingofchilling-sensitiveplants(Hariyadi,Parkin,1993;Prasadetal.,1994b).

Minorsky(1985)proposedahypothesis toex-plain most of the secondary effects of chilling shock,whichsuddenlyincreases(by1–2orders)intheconcen-trationof[Ca2+]cyt.Itisassumedthattherapidincreasein[Ca2+]cytduetochilling,mayserveastheprimaryphysio-logicalsignalofcoldexposure.Itwasshownthatchang-es in intracellular calcium compartmentation in chilledplants,leadingtoanincreasein[Ca2+]cyt,stopcytoplasmicstreaming andaffect thesubcellularstructures (Woodsetal.,1984b).Thereisevidencethatinputof45Ca2+ inmaizerootcellsincreasedby20–25%atatemperatureof2°C(Zocchi,Hanson,1982).Changesin[Ca2+]cyttriggercascade reactions in the cell,which leads to numerousdisturbancesatalllevelsofanorganization.Ourinves-tigationshowsthatchillinginducesabruptreductionofCa2+-ATPaseactivity,whichpumpsoutCa2+inapoplastand/or in intracellular depots (Лукаткин, Еремкина,2002).So,thisenhancesthe[Ca2+]cytlevelincytoplasm.DuringthegrowthofmaizeseedlingsonnutrientmediawithdifferentcalciumstatusmoreintensechillinginjurywasobservedatreducedorenhancedCa2+dosesincom-parisonwithoptimaldose(Lukatkin,Isaikina,1997).

In recent years, the calcium hypothesis hasbeen furtherdeveloped inviewofoxidative stress thatoccurswhencoolingthechilling-sensitiveplants.Oxida-tivestressthatoccursduringcoolingofchilling-sensitiveplantsplaysaleadingroleinthetransductionofchillinginjury(Lukatkin,2002a;b;Huetal.,2008).Thereasonwhyproductionoffreeradicalsandreactiveoxygenspe-cies(ROS)increasedissingletoxygen,superoxideanion,hydroxyl radical, hydrogen peroxide (Suzuki, Mittler,2006).TheseROScauseconsiderabledamage tomem-brane lipids and other cellular components (Lukatkinet al.,1995;Lukatkin,2003;Поповидр.,2010).Itwasshownthat[Ca2+]cytchangesareintimatelyconnectedtoan oxidative stress.Oxidative stress causes an immedi-ateincreaseincytosoliccalcium(Priceetal.,1994),act-ingthesameaschillingshock(Knightetal.,1996).Thisreactionistransient,andfinisheswithin1–2minutes.Inturn,[Ca2+]cytinfluencesaleveloffreeradicals,inhibitingactivity of SOD (Price et al., 1994). So, increasing theconcentrationofionizedcalciumcausesincreasedoxida-tivestress(Priceetal.,1994;Lock,Price,1994),i.e.isthesignalamplificationcascadethatcauseschillingdamage.

Summarizedschemeoftheinitiationanddevel-opment of chilling injury in the cells of chilling-sensi-tiveplantsisshowninFigure.Thisschemeincludesallphysiologicalandbiochemicaleventswhichareknownaschillingdamageofsusceptibleplants.

ISSN 1392-3196 ŽEMDIRBYSTĖ=AGRICULTURE Vol.99,No.2(2012) 117

Ways to improve chilling toler-ance of chilling-sensitive plants Atthepresenttime,toimprovethechillingtol-

erance of sensitive plants various techniques are used,whichcanbedividedintoseveralgroups:thethermalef-fect,chemicaltreatment,theuseofcellularandgeneticengineering.

Thermal effectsincludeslow-temperaturehard-ening,thermalconditioning,intermediatewarming,andtheeffectofheatstress.Thebasisofseedandseedlinghardeningofchilling-sensitiveplantstocold,whichhaslongbeenusedinpracticalplantbreeding,istheadapta-tionoftheorganismintheearlystagesofdevelopment,accompaniedbytheemergenceofspecificstructuralandfunctionalrearrangements(Генкель,Кушниренко,1966,Дроздовидр.,1977).Low-temperaturehardeningproc-ess is associated with the protein-synthesizing system(Титов,Шерудило,1990)andisaccompaniedbyarear-rangementofthehormonalsystemofplants(Талановаидр.,1991;Волковаидр.,1991).

Similartothehardeningisthethermalconditio-ning(“preconditioning”),associatedwithchangesinplantresponsetochillingconnectedwithgrowthtemperatureintheprecedingperiod.Growingplantsat lower tempera-tures leads to acclimation, which increases their resis-tance tochilling (Nieetal.,1992;Leipneret al.,1997;Kingstom-Smithetal.,1999;Leipneretal.,2000;Kato-Noguchi,2007;Поповидр.,2010),aswellasexposureofchilling-sensitiveplantsortheirtissueforsomeperiodoftime(from2to14days)toarelativelyreducedtem-peratures(10...18°C)(Wolk,Herner,1982;Wang,1982;

Ahnetal.,1999).Suchconditioninggives theplantsagreaterdegreeofchillingtoleranceforsometime(Bolgeretal.,1992;Cabaneetal.,1993;Capell,Dörffling,1993;Andersonetal.,1994;Wangetal.,1992;Wang,1993;1995). Conditioning causes changes in physiologicalandbiochemicalprocesses inplants,changesoperationof protein-synthesizing system, leads to the synthesisofnewproteins,possiblyinvolvedinprotectionagainstchilling shock (Marangoni et al., 1990; Cabane et al.,1993;Andersonetal.,1994;Prasadetal.,1994a).Thethermal conditioning is dependent on temperature andlightinthisperiod(Grishenkovaetal.,2006;Лукаткинидр.,2006).

Intermediate warming is another way of ther-malregulationofchillinginjury.Transferofthechilledplants in thewarmafternoonprevented theappearanceofvisible symptomsofdamage, impaired inhibitionofphotosynthesis and transpiration, reduced leaf osmoticpotential(Koscielniaketal.,1996;Koscielniak,Biesaga-Koscielniak, 2000; Skrudlik et al., 2000). Intermediatewarming is often used for storage of chilling-sensitiveplants’fruits(Wang,1982;1993).Itisassumedthatthetemporaryplacementinheatallowsthechilledtissuestometabolize toxicsubstances thataccumulateduring thechillingprocess,orhelpstorestorethecompoundsintis-suesthataredepletedduringchilling(Lyons,1973).

High-temperatureconditioning(heatingforseve-ralminutes)ofseedsandseedlingsinducedincreasedchill-ing-resistanceinplants(Rab,Saltveit,1996b;Mandrich,

Figure.Schemeoftheinitiationanddevelopmentofchillinginjuryinthecellsofchilling-sensitiveplants

118 Chilling injury in chilling-sensitive plants: a review

Saltveit, 2000).This process involves protein synthesis.So,intissuesexposedtoheatstressthereisobservedtheappearance of newmRNAs and proteins that aremain-tainedandevenincreasedafterchilling,butquicklydis-appearat theoptimum temperature (Adnanet al., 1998;Kadyrzhanovaetal.,1998;Sabehatetal.,1998).

Chemical treatmentsofchilling-sensitiveplantsleadtoincreasedchillingtolerance.Theeffectsoftraceele-ments,syntheticgrowthregulators,andantioxidantsweremoststudied.Onegroupofcompounds,themostpromis-ingintermsofincreasingthechillingresistanceofchilling-sensitiveplantsissyntheticanaloguesofphytohormonesandotherplantgrowthregulators.Theefficacy,whichin-ducedanincreasedresistancetochillingwasshownforallgroupsofphytohormones(Генкель,Кушниренко,1966;Володько,1983;Зауралов,Лукаткин,1996).

CytokininsandABAweremosteffectiveofallplantgrowthregulators(Duncan,Widholm,1991;Mitch-ell,Madore,1992;Andersonetal.,1994;Pareeketal.,1997;Заураловидр.,2000;Lukatkinetal.,2003;Lu-katkin,Zauralov,2009;Лукаткин,Овчинникова,2009).Non-hormonalgrowthregulatorsareusedalso inorderto improve the chilling tolerance of cultivated plants.These includepaklobutrazol, chlorocholinchloride,me-fluidid,unikonazolandothertriazoles(Lurieetal.,1994;Feng et al., 2003).The treatment by antioxidants andfree radicals quenching (ethoxyquin, sodium benzoate,glutathione, tyrone, formate, ascorbate, diphenylamine,α-tocopherol,propylgallate)canslowdownthedegrada-tionofunsaturatedfattyacidsandreducechillingdam-ageinchilling-sensitiveplants,leavesandfruits(Lukat-kin,Levina,1997;Michaelietal.,1999;Xuetal.,2000;Kocsyetal.,2001).Increasingthechillingresistanceofchilling-sensitiveplantsisalsoshownforcompoundsofdifferent nature: choline, proline, polyamines, glycinebetaine, alcohols, anesthetics, etc. (Lyons et al., 1979;Wang, 1982; Duncan, Widholm, 1991; Wang, 1993;Frenkel,Erez,1996;Jandaetal.,1999;Shenetal.,2000;Dingetal.,2007;Wangetal.,2008b).Themechanismsoftheiractionaredifferent.Theyincreasethefluidityofmembranes,protectingthemfromfreeradicalperoxida-tion,altertheratiooflipidaswellasproteinconforma-tion,therebyalteractivityofmembraneenzymes,influ-encehormonessynthesis,waterregime,etc.

Cellular and genetic engineeringisanewtrend,whichallowsfundamentalchangesinthechillingresist-anceofchilling-sensitiveplants.Theyarebasedonalargegeneticvariabilityincomponents,controllingsensitivity,ontheonehand,andonthedevelopmentofgenetransfertechnology,transformationandselectionmarkers,ontheotherhand(Greaves,1996;Лукаткин,Дерябин,2009).So,screeningthesurvivingcellsduringchillingofcallusandsuspensionculturesandsubsequentplantregenera-tionyieldedplantswith increasedepigenetic resistancetochillingtemperatures(Dix,1979;Lukatkin,1999;Lu-katkin,Geras’kina,2003;Lukatkin,2010).Somatichy-bridizationmaybeaconvenientwayfortheintroductionofgermplasm,associatedwith resistance tochilling, innewlinesoftomato(Bruggemannetal.,1995;Venemaetal.,2000).The increasedchilling toleranceobserved

intransgenictobaccoplantswithintroducedchloroplastω-3 fatty acid desaturase from Arabidopsis thaliana or Δ9-desaturase from the cyanobacterium Anacystis nidulanswithincreasedlevelsofpolyunsaturatedfattyacidsinmembranelipids(Kodamaetal.,1994;Ishizaki-Nishizawaetal.,1996;Hamadaet al.,1998;Murata,Ta-saka,1997).

Conclusion The literature review shows that the exposure

ofchilling-sensitiveplantstolowtemperaturesleadstodisturbances in all physiological processes –water re-gime,mineralnutrition,photosynthesis, respirationandmetabolism. Inactivation of metabolism, observed atchillingofchilling-sensitiveplantsisacomplexfunctionofbothtemperatureanddurationofexposure.Responseofplantstolowtemperatureexposureisassociatedwithachangeintherateofgenetranscriptionofanumberoflowmolecularweightproteins.

Basedontheauthors’ownresearchandthelite-raturedata, the conceptof colddamagewasproposed,which highlighted the leading role of oxidative stressin the induction of stress response. According to thisconcept, thereweredistinguishedpossibleways to im-provecoldtolerance,whichwerecombinedintoseveralgroups: the thermal effect (low-temperature hardening,thermalconditioning,intermediatewarmingandtheef-fectofheatstress),chemical treatment(traceelements,syntheticgrowthregulators,antioxidants)andtheuseofgeneandcellengineering.

Acknowledgements This research was supported by the RussianMinistryofEducationandScienceundertheAnalyticalDepartmentalTargetProgram“DevelopmentofScientistPotentialofHigherSchool”,ProjectNo.2.1.1/624. Thisworkwascarriedoutwithintheframeworkofthelongtermresearchprogram“Horticulture:agro-bio-logicalbasicsandtechnologiesimplementedbyLithua-nianResearchCentreforAgricultureandForestry”.

Received25112011Accepted06022012

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ISSN 1392-3196 Žemdirbystė=Agriculture,vol.99,No.2(2012),p.111‒124UDK634.1:581.17:576.3

Žemų temperatūrų poveikis jautriems augalams: apžvalgaA.S.Lukatkin1,A.Brazaitytė2,Č.Bobinas2,P.Duchovskis2

1Mordovijosvalstybinisuniversitetas,Rusija2LietuvosagrariniųirmiškųmokslųcentroSodininkystėsirdaržininkystėsinstitutas

SantraukaŽemosteigiamos(1–10°C)temperatūrossąlygojadaugybęfiziologiniųsutrikimųtokiomstemperatūromsjautriųaugalųląstelėse,otailemiatropiniųirsubtropiniųaugalų,pavyzdžiui,daugeliodaržovių,žūtį.Literatūrosapžvalgaparodė,kadšilumamėgiųaugalųlaikymasžemųteigiamųtemperatūrųsąlygomisnulemiavisųfiziologiniųprocesų(vandensrežimo,mineralinėsmitybos,fotosintezės,kvėpavimo,medžiagųapykaitos)pažeidimus.Šilumamėgiųaugalųmedžiagųapykaitos inaktyvacija,nustatytažemųtemperatūrųsąlygomis,priklausoirnuotemperatūros,irnuojostrukmės.Augalųatsakasįžemųteigiamųtemperatūrųpoveikįyrasusijęssukeletomažosmolekulinėsmasėsbaltymųgenųtranskripcijosgreičiu.Apžvalgojeanalizuojamižemųtemperatūrųpažeidimųsampratoskaitosistoriniaiaspektaiiršiuolaikiniųtyrimųkryptys. Remiantis autorių tyrimais ir literatūros duomenis, pasiūlyta žemų teigiamų temperatūrų pažeidimųkoncepcija,pagalkuriądidžiausiareikšmėtenkaoksidaciniamstresuikaipstresinėsreakcijossukėlėjui.Pagalšiąkoncepcijąpasiūlytikelibūdai,kaippadidintižemųtemperatūrųtoleranciją.Jiesuskirstytiįkeliasgrupes:terminispoveikis (grūdinimas žemomis temperatūromis, temperatūrinis kondicionavimas, tarpinis atšildymas, šilumosstreso poveikis), cheminis apdorojimas (mikroelementais, sintetiniais augimo reguliatoriais, antioksidantais) irgenųbeiląsteliųinžinerijospanaudojimas.

Reikšminiai žodžiai: antioksidantai, fiziologiniai procesai, ląstelės, oksidacinis stresas, žemoms teigiamomstemperatūromsjautrūsaugalai.

Chilling injury in chilling-sensitive plants: a review