Differences in chilling sensitivity of cucumber varieties depends on storage temperature and the...

Postharvest Biology and Technology 17 (1999) 97–104

Differences in chilling sensitivity of cucumber varietiesdepends on storage temperature and the physiological

dysfunction evaluated

Abdul Hakim a, Albert C. Purvis a,*, Ben G. Mullinix b

a Department of Horticulture, The Uni6ersity of Georgia, Coastal Plain Experiment Station, Tifton, GA 31793-0748, USAb Experimental Statistics Unit, The Uni6ersity of Georgia, Coastal Plain Experiment Station, Tifton, GA 31793-0748, USA

Received 8 March 1999; received in revised form 17 April 1999; accepted 12 June 1999

Abstract

Fruit from eight Plant Introduction (PI) lines, 12 F1 hybrids of crosses between chilling-sensitive and chilling-resis-tant lines and two commercial cultivars of cucumber (Cucumis sati6us L.) were stored for 7 days at 1 or 4°C followedby 2 days at 24°C and evaluated for chilling injury. The chilling-induced symptoms and physiological dysfunctionscompared included visible pitting, decay, weight loss during storage at low temperature, electrolyte leakage,chlorophyll fluorescence ratios, respiration rates and pyruvate accumulation in the mesocarp tissue. Severity ofchilling-induced injury among the lines, hybrids and cultivars depended on the particular symptom or physiologicaldysfunction examined. Fruit from all lines, crosses and cultivars exhibited greater injuries after storage at 1°C thanafter storage at 4°C. Other than visible pitting and decay, only small, sometimes indistinguishable, differences wereobserved among the various lines as to their sensitivity to low temperatures. In this study, chlorophyll fluorescenceratios proved to be of little value in distinguishing between chilling-sensitive and chilling-resistant lines of cucumber.Decay and weight loss were the only measurements that were significantly correlated with chilling-induced visiblepitting. Respiration rates were correlated with weight loss, but not with visible pitting and decay, during storage at1 and 4°C. It is concluded that low temperatures do not affect all biochemical and physiological processes ofcucumber to the same extent. Furthermore, there is a continuum of sensitivity of each process to low temperature,and whether a cultivar is deemed to be chilling-sensitive or chilling-resistant depends on which particular biochemicalor physiological process is evaluated. © 1999 Elsevier Science B.V. All rights reserved.

Keywords: Cucumis sati6us L.; Visible pitting; Decay; Weight loss; Chlorophyll fluorescence ratios; Respiration; Electrolyte leakage;Pyruvate

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1. Introduction

Cucumbers, Cucumis sati6us L., like manywarm-season horticultural crops, are injured whenthey are exposed to temperatures just above freez-

* Corresponding author. Tel.: +1-912-386-3900; fax: +1-912-386-3356.

E-mail address: [email protected] (A.C.Purvis)

0925-5214/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved.

PII: S 0925 -5214 (99 )00037 -X

A. Hakim et al. / Posthar6est Biology and Technology 17 (1999) 97–10498

ing. While cucumber seeds apparently are notinjured when imbibed at low temperatures(Herner, 1986), germinated cucumber seedlingsare injured if they are exposed to low tempera-tures for several hours (Cabrera et al., 1992;Smeets and Wehner, 1997) and the harvested fruitare injured when they are stored at low tempera-tures for a few days (Cabrera et al., 1992; Mercerand Smittle, 1992; Purvis, 1994, 1995). Geneticvariation among cultivars and germplasm of cu-cumbers exists for the ability to germinate at lowtemperature (Smeets and Wehner, 1997) and forresistance to chilling injury in both seedlings andfruit (Cabrera et al., 1992; Purvis, 1995; Smeetsand Wehner, 1997). The susceptibilities to chillinginjury of seedlings and fruit of the same cucumbercultivar, however, do not appear to be highlycorrelated (Cabrera et al., 1992). This may be dueto the influence of environmental conditions,other than temperature, during and prior to expo-sure to low temperature on the severity of injury(Rietze and Wiebe, 1989; Mercer and Smittle,1992; Smeets and Wehner, 1997).

Relative humidity has a significant influence onthe development of chilling-injury symptoms inseedlings and in fruit during postharvest storage.The earliest visible evidence of chilling injury incucumber fruit is sinking of the spines, which maybe broken during harvest, followed by water-soaking and the formation of pits in other areason the fruit surface (Morris and Platenius, 1939).The severity of pitting is inversely related to therelative humidity of the storage atmosphere. Mor-ris and Platenius (1939) suggested that the re-duced transpiration rate, rather than the highhumidity itself, is the effective factor in minimiz-ing injury caused by low temperatures. Tasumi etal. (1987) suggested that pitting of cucumber fruitis associated with cracks in the cuticle and sinkingof epidermal cells near the stomates, which leadsto an enhanced transpiration rate. Water loss andthe development of chilling-injury symptoms ingrapefruit and lemons were associated with micro-scopic cracks in the cuticular waxes around thestomates of fruit stored at low temperatures (Co-hen et al., 1994). Moisture loss at non-chillingtemperatures, however, does not result in the dis-tinct pitting characteristic of chill-injured fruit,

but rather in a general shriveling of the entirefruit.

Chilling-induced pitting of fruit from 64 PIlines of cucumbers was highly correlated with theweight lost during low-temperature storage(Purvis, 1995). The fruit from some lines, how-ever, did not pit even though they lost moisture atrates similar to those which pitted severely, whilethe fruit from other lines pitted, but lost littlemoisture during storage. Thus, it appears thatalthough moisture loss enhances pitting, it is notthe primary cause of pitting. The question then iswhether cucumbers that do not pit are still chill-injured when they are exposed to low tempera-tures. In addition to pitting, chill-injuredcucumber fruit are more susceptible to decay(Morris and Platenius, 1939), have higher respira-tion and ethylene production rates (Eaks andMorris, 1956; Cabrera and Saltveit, 1990; Cabreraet al., 1992), higher chemical and ion leakage rates(Fukushima et al., 1977; Fukushima andTsugiyama, 1977; Cabrera and Saltveit, 1990;Cabrera et al., 1992) and decreased chlorophyllfluorescence ratios (Tijskens et al., 1994). Thepurpose of this study was to compare the relation-ship between pitting and other physiological man-ifestations of chilling injury in cucumber fruit.Fruit from two commercial cultivars whose fruit,but not their seedlings, differed in their suscepti-bility to chilling injury (Cabrera et al., 1992;Smeets and Wehner, 1997), as well as some of thechilling-susceptible and chilling-resistant PI linesand F1 hybrids of crosses between susceptible andresistant lines from a previous study (Purvis,1995) were used.

2. Materials and methods

Cucumber (C. sati6us L.) seeds of the two com-mercial cultivars, eight PI lines from several coun-tries and 12 F1 hybrids were planted in the field atthe Coastal Plain Experiment Station, Universityof Georgia, Tifton, GA. The seeds of the PI lineswere obtained from the Plant Introduction Sta-tion, Ames, IA, and crosses between lines withsimilar fruit morphological characteristics weremade in the greenhouse to obtain seeds of F1

A. Hakim et al. / Posthar6est Biology and Technology 17 (1999) 97–104 99

hybrids between lines which exhibited resistanceand lines which were susceptible to chilling injury(Purvis, 1995). The seeds were germinated in flatsin the greenhouse and then transplanted in thefield, where they were grown using standard horti-cultural practices. Seeds from some of the crosseseither failed to germinate or did not produceseedlings that survived in the field.

Fruit were harvested when they appeared to bemature. Only fruit with no visible external defectswere stored. The fruit were rinsed with tap water,air dried, labelled and then stored in kraft paperbags open to the atmosphere for 7 days in dark,ventilated rooms at 1 or 4°C followed by 2 days at24°C. Five to 15 fruit, depending on the numberof fruit available from each line at harvest, wereused.

Fruit were weighed before storage, immediatelyafter storage and 2 days after transfer to roomtemperature (24°C). Weight loss was calculated asa percentage of initial fresh weight.

Chilling-injury evaluations were made after 1 or2 days at 24°C following removal from storage at1 or 4°C. Visible pitting and decay ratings weremade on a scale of 1–5, with: 1, no injury; 2,1–10% of the surface injured; 3, 11–25% of thesurface injured; 4, 26–50% of the surface injured;5, \50% of the surface injured.

Chlorophyll fluorescence was measured with aPlant Efficiency Analyzer (Hansatech, UK). Thefruit were marked where the fluorescence mea-surement was performed to ensure that subse-quent readings could be taken from the samelocation of each fruit. The fruit were placed in adark room for 20 min before fluorescence mea-surements were taken. The fluorescence probewith a light intensity of 20 mmol m−2 s−1 wasplaced firmly against the fruit in the markedareas. Fluorescence measurements were recordedfrom the fluorescence digital display and trans-ferred to a computer software program foranalysis.

Triplicate samples of three cucumber fruit fromeach treatment were used to determine respiratoryrates 1 day after removal from low-temperaturestorage. The fruit were weighed and placed in a4-l sealed plastic container at 24°C. The increasein the CO2 concentration during timed intervals

was measured with a Nova CO2 analyzer (NovaAnalytical Systems, Inc., New York, USA) andused to calculate rates of respiration.

Electrolyte leakage was measured with tissuetaken from three randomly selected fruit fromeach treatment on the second day after removalfrom low-temperature storage. Five disks (7-mmdiameter) of mesocarp tissue were removed fromeach fruit with a cork borer. The disks were rinsedthree times in deionized water and placed in 10 ml0.4 M mannitol in culture tubes at 24°C. Electri-cal conductivities of the solutions were deter-mined after 3 h with a conductance meter (Model32, Yellow Springs Instrument Co., OH, USA).Afterwards, the samples were autoclaved at 120°Cfor 20 min, cooled, and a final conductivity read-ing was taken for total tissue electrolytes. Leakagedata are expressed as a percentage of the totalelectrolytes.

Pyruvate content of the mesocarp tissue of cu-cumber fruit was determined by enzymatic assayon the same fruit that were used for electrolyteleakage assays. Fresh tissue was taken from threefruit of each treatment and homogenized (15 gtissue plus 12 ml deionized water) with a Waringblender for 15 s at low speed. After adding 2 mltrichloroacetic acid solution (0.375 g ml−1), thehomogenate was allowed to stand for 15 min atroom temperature and then it was filtered. Fiftymicroliters of the supernatant were transferred toa culture tube and underlaid with 3.95 ml 0.5 Mtris buffer. A blank and a pyruvate standard (32mM) were similarly prepared. The tubes wereheated at 40°C for 5 min. Two-milliliter sampleswere removed to cuvettes and 25 ml of 20 mMNADH were added. Absorbance at 340 nm wasrecorded before and 5 min after adding 10 ml 1000U ml−1 lactic dehydrogenase. The concentrationof pyruvate was calculated as nmol g−1 freshweight.

Data were subjected to analysis of varianceusing PROC MIXED (SAS Institute, 1992). For therating data, visible pitting and decay, means weredetermined for each variety at each temperature.The least-squares difference (LSD) at P=0.05was determined on the 22 differences between thetemperatures for each variety. The Fisher’s LSDmean separation test was used to assign letters to


the remaining data. Due to various sampling tech-niques that were used, correlations were per-formed on all the individual cucumber data(N=129), laboratory data (N=66), and betweenthe two groups of variety means (N=22) for eachtemperature.

3. Results and discussion

Fruit from the PI lines were classified either asresistant or susceptible to chilling-induced pitting

based on results of a previous study (Purvis,1995). Fruit from all of the PI lines, the F1

hybrids and the two commercial cultivars devel-oped some visible pitting after storage at either 1or 4°C for 7 days followed by 2 days at 24°C(Table 1). The ranking of the PI lines for chillingsusceptibility based on the amount of visible pit-ting was similar to the ranking observed in theprevious study (Purvis, 1995). Pitting was moresevere (PB0.01) on fruit stored at 1°C, with amean rating of 3.4, compared with those at 4°C,with a mean rating of 2.4. The degree of pitting

Table 1Visible pitting, decay, weight loss (during storage), and chlorophyll fluorescence ratio means of cucumber fruit stored at 1 or 4°Cfor 7 days followed by 2 days at 24°C

Chlorophyll fluorescence ratiobWeight loss (%)Varietya PittingbN Decayb

4°C 1°C 4°C1°C 4°C 1°C 4°C 1°C

0.40 efgh2.6 gh1.9 ef1.0 0.78 ab1.11.2+1.310K32c

1.0 2.2 cdef 2.8 fgh 0.35 ghi 0.79 ab2.0 1.3K114 1.06HLGV 0.75 abcd0.50 bcdef5.4 a*2.7 bc1.01.02.2+2.45

4.3 bcd 0.56 abcd 0.77 abc1.4 *2.1 cdef1.42.23.65MU4.4 bc 0.39 efghiE 5 0.71 abcdef4.4 + 4.2 2.8 1.8 3.2 b

5 5.0 * 3.0 4.2 *A 2.2 0.72 abcde0.57 abc3.2 fgh2.6 bc0.64 ef+0.69 a5.0 ab4.0 a5 5.0 * 3.2 2.0 1.2K

2.83.65.05 1.8T2 2.6 bcd 3.0 fgh 0.43 defg 0.65 ef2.4 cdef5 2.6 gh 0.36 fghi 0.70 abcdef4.8 * 3.2 1.8 1.4NS×MU2.3 cdef5 2.6 gh 0.49 bcdefg 0.78 ab3.0 2.0 2.4 * 1.2E×HLGV

0.80 ab0.66 a2.9 fgh2.2 cdef1.7H×K32 2.42.13.010* 4.3 bcdT2×HLGV 0.48 bcdefg5 0.79 ab3.4 2.6 1.4 1.2 3.1 b

2.6 bcde 2.8 fgh 0.77 abc0.51 bcde1.82.63.85HKC×HLGV 1.04.5 bc 0.44 cdefg 0.80 a1.8 *2.4 cdefA×HLGV 5 4.2 3.0 2.8

5 3.3 efgh 0.61 ab + 0.61 f2.4 + 2.2 1.6 1.2 2.6 bcMU×NS1.8 f5 2.9 fgh 0.44 cdefg 0.68 ab3.4 2.2 2.2 1.4K114×H

1.2 2.7 bc 3.6 cdef 0.45 cdefg 0.80 aMU×K 5 3.8 * 2.2 2.21.6 2.4 cdef 3.1 fgh 0.27 hi * 0.62 efHLGV×HKC 5 4.2 3.4 3.2 *

0.66 def*0.25 i4.2 bcde3.2 b1.2HLGV×T2 2.02.8*4.453.4 defg 0.48 bcdefg 0.79 abK32×H 5 4.8 * 2.2 2.2 1.8 2.7 bc

1.1 1.8 f 0.44 cdefg 0.70 bcdefP76 3.0 fgh15 2.5 + 2.3 1.32.5 h 0.45 cdefg 0.70 abcdef1.0 1.9 def2.65M76 1.6 1.4

131 3.4 0.47 0.733.4 * 2.4 1.9 1.4 2.4Mean2.14 0.92 0.146 0.439LSD (0.05) 0.57 0.62 0.67

a K32, Kecskemeti 32 and K114, Kecskemeti 114 (Hungary); HLGV, Hollandse Lange Groeme VO (Netherlands); MU,Monastyrski, Ulrich (Poland); E, Esvier and A, Amato (Netherlands), Kirak (Pakistan); T2, T2 (Netherlands); NS, Nochowski,Szklarniowy (Poland); HKC, Hybrid KC 291 (Netherlands); H, 2700817 (Hungary); P76, Poinsett 76; M76, Marketmore 76.

b Visible pitting and decay ratings on scale of 1–5: 1, no injury; 2, 1–10% of surface injured; 3, 11–25% of surface injured; 4,26–50% of surface injured; 5, \50% of surface injured; and Cf ratio=Fv/Fm.

c Means followed by the same letter are not significantly different according to Fisher’s least-squares difference (LSD) (P=0.05).* and + denote significant differences between the two temperatures, where * is greater than the mean difference, while + is smallerthan the mean difference.


Table 2Correlation coefficients for various chilling injury parameters of cucumber fruit stored for 7 days at 1 or 4°C followed by 2 daysat 24°Ca

DC WL FL ELVPb RS4°C 1°C 4°C 1°C 4°C 1°C1°C 4°C 1°C 4°C 1°C 4°C

0.34**DC 0.61**0.34** 0.30** 0.070.54**WL

−0.19* −0.02 −0.11 0.10 −0.02FL −0.020.27 −0.36 −0.01 0.35 0.11 0.10−0.10 0.17EL0.15 −0.20 0.13RS 0.44*0.15 0.53* 0.04 0.13 0.30* −0.060.02 −0.29 −0.13 0.12 0.48* 0.23 −0.06 0.16 0.16 0.27*−0.14 0.09PY

a N=129 (VP, DC, WL, FL), N=66 (EL, RS, PY) and N=22 [(VP, DC, WL, FL)�(EL, RS, PY)]. * and ** denote significancelevels of P=0.05 and P=0.01, respectively.

b VP, visible pitting; DC, decay; WL, weight loss (%); FL, chlorophyll fluorescence ratio; EL, electrolyte leakage; RS, respiration;PY, pyruvate content (%).

on fruit from the F1 hybrids was intermediatebetween the two parents regardless of which par-ent exhibited chilling resistance. Three of the PIlines had nearly the same rating, while two of thePI lines had ratings that were about two cate-gories apart. Only one F1 hybrid had nearly thesame rating, while four F1 hybrids had ratingsthat were about two categories apart. Only onecommercial line had nearly the same rating.

Decay ratings followed a pattern similar to thatof visible pitting ratings, but there was less differ-ence (P\0.10) in decay ratings between resistantand susceptible lines than there was in pittingratings (Table 1). Only one PI line and two hy-brids had ratings that were significantly greaterthan the mean difference between the tempera-tures. Decay ratings and pitting ratings, however,were significantly correlated for fruit stored at1°C (0.61**) and at 4°C (0.34**) (Table 2). This isin contrast to the study by Cabrera et al. (1992)reporting a poor correlation between pitting anddecay among cultivars. However, Cabrera andSaltveit (1990) suggested that pitting and decayare inter-related since breakdown of the tissueprovides a suitable environment for the growth ofsaprophytic pathogens that colonize chilled cu-cumber fruit.

In a previous study (Purvis, 1995), weight lossduring low-temperature storage was correlatedwith visible pitting developing on the fruit. Al-though transpiration rates are proportional to thevapor-pressure deficit and the permeability of the

epidermis to water vapor, circulation of air en-hances the rate of transpiration because it reducesthe moisture-saturated boundary layer on thefruit surface. Circulation of air in the storageroom might account for some of the differencesobserved in weight loss and amount of pittingbetween the two seasons reported by Purvis(1995). In the present study, the fruit were storedin kraft paper bags that were open to the atmo-sphere to reduce the air circulation effect ontranspiration. Under these conditions, weightlosses were still correlated with the subsequentdevelopment of visible pitting on fruit stored at1°C (0.54**) and at 4°C (0.34**) (Table 2).Weight losses were greater (P\0.05) at 4°C thanat 1°C (Table 1). Although the difference of 1%between the means of the temperatures was notsignificant, there were two PI lines and two F1

hybrids where the variety difference between thetemperatures were significantly greater. Both F1

hybrids had Hollandse Lange Groeme VO(Netherlands) (HLGV) as a parent, which alsohad a greater difference. In support of the conceptthat chilling-induced pitting of cucumber fruit isassociated with moisture loss during low-tempera-ture storage are results showing that cucumberfruit coated with surfactant-based waxes whichenhanced moisture loss developed more visiblepitting at 5°C than unwaxed fruit or fruit coatedwith waxes that retarded moisture loss (Purvis,1994). Mack and Janer (1942), however, reportedmore severe pitting on waxed cucumber fruit than


on unwaxed fruit, even though the waxed fruitlost less weight. They suggested that low-tempera-ture-induced pitting is related to suboxidation inview of the significant increase in the respiratoryquotient in cold-stored waxed cucumber fruit.Chill-injured cucumber fruit exhibit increased res-piratory rates (Eaks and Morris, 1956).

The destruction of photosystem II in chloro-phyllous tissue has been related to the peroxida-tive deterioration of cell membranes duringchilling stress (Tijskens et al., 1994). The quantumyields of photosystem II, measured with pulseamplitude modulated chlorophyll fluorescenceand expressed as chlorophyll fluorescence ratios(Fv/Fm), were remarkably uniform for the fruit ofa particular line prior to storage (0.83\Fv/Fm\0.74) and changed little in some of the linesduring 7 days of storage at 4°C (Table 1). Incontrast, large decreases in Fv/Fm occurred incucumber fruit of most of the lines stored for 7days at 1°C. Although the temperature differencewas a reading of 0.26Fv/Fm less for 1°C than for4°C (PB0.01), there were two, one PI line andone F1 hybrid, that had nearly the same reading,while there were two F1 hybrids that had signifi-cantly greater difference in readings. Two of theF1 hybrids also had HLGV as a parent, but theparent had a difference close to the mean of allthe varieties. Thus, the decrease in Fv/Fm appearsto be more a function of the storage temperaturethan of cultivar. Fv/Fm was correlated only withvisible pitting at 4°C (−0.19*) (Table 2).

Respiration rates were higher for fruit whichhad been stored at 1°C than for fruit which hadbeen stored at 4°C (P\0.05), indicating greaterchilling injury at 1°C than at 4°C (Table 3). Notethat HLGV T2 (Netherlands) (HLGV×T2) hadthe highest values at both temperatures (2.7 dif-ference, mean=14.3), and Esvier HLGV (E×HLGV) had the lowest values at bothtemperatures (6.8 difference, mean=14.3). Noneof the 22 varieties had a difference that wassignificantly greater than the mean difference.Both variety Amato (Netherlands) and T2 valuesfor 1°C were less than for 4°C. Respiration rates,however, were not correlated with visible pittingamong the PI lines, F1 hybrids and the two com-mercial cultivars. Respiration rates were corre-

lated with weight loss for fruit that had beenstored at 1°C (0.44*) and at 4°C (0.53*) (Table 2).Respiration rates were also correlated with pyru-vate levels in cucumber fruit stored at 1°C (0.27*)but not at 4°C (Table 2).

Pyruvate, the end product of glycolysis, accu-mulated to higher levels (PB0.01) in the meso-carp tissue of cucumber fruit stored at 1°Ccompared with fruit stored at 4°C (Table 3). Thegreater accumulation of pyruvate in tissues fromfruit stored at 1°C than from those stored at 4°Creflects the higher respiration rates observed at1°C than at 4°C. The mean difference in pyruvatevalues was 104. There were one PI line and threeF1 hybrids with differences that were significantlygreater. There were two PI lines and one F1

hybrid with differences that were significantlysmaller. Pyruvate was previously reported to ac-cumulate in cucumber and chilling-sensitive egg-plant fruit stored at 1°C, but not at 5 or 20°C(Tsuchida et al., 1990). The activity of pyruvatekinase, which converts phosphoenol pyruvate topyruvate, is highly allosterically regulated by in-termediates and products of respiratorymetabolism. Pyruvate kinase loses its sensitivity toallosteric control at low temperatures (Llorente etal., 1970) and pyruvate can accumulate in tissuesat low temperatures. Pyruvate is a transientmetabolite that is metabolized through severalpathways (Purvis, 1997). One metabolic fate ofpyruvate is its transamination to alanine. Alanineis also an allosteric inhibitor of pyruvate kinaseand the loss of sensitivity of pyruvate kinase toallosteric control at low temperatures can accountfor the accumulation of alanine in cucumber fruitstored at low temperatures (Kozukue et al., 1984)as well as in tissues of other chilling-sensitivespecies exposed to low temperatures (Patterson etal., 1981).

Electrolyte leakage was higher (PB0.01) forfruit that had been stored at 1°C than for fruitthat had been stored at 4°C (Table 3). Two PIlines and five F1 hybrids had values that weresignificantly greater (P=0.05) from the mean dif-ference of all the varieties. There was one PI linethat was significantly less (P=0.05) and its 1°Cvalue was almost 25% of the 4°C value. Theinfluence of temperature and duration of chilling


exposure on electrolyte leakage by chilling-sensi-tive tissues apparently is species dependent. Incontrast to cucumber (Fukushima andTsugiyama, 1977; Murata and Tatsumi, 1979;Cabrera et al., 1992) and tomato (King and Lud-ford, 1983; Autio and Bramlage, 1986) fruit inwhich chilling enhances electrolyte leakage, bellpepper and eggplant (Murata and Tatsumi, 1979)and yellow summer squash (McCollum, 1989) donot exhibit an increase in electrolyte leakage inresponse to chilling stress. In the present study,

electrolyte leakage rates were variable and werenot correlated with visible pitting of fruit stored at1 or 4°C, but were correlated (P\0.05) withweight loss of fruit stored at 1°C but not at 4°C(Table 2). Thus, the role of electrolyte leakage inthe development of visible pits during chilling isquestioned.

The severity of chilling-induced injury of cu-cumber fruit varied among the various lines, hy-brids and cultivars, depending on the particularvisible symptom or physiological dysfunction ex-

Table 3Respiration, electrolyte leakage, and pyruvate means of cucumber fruit stored at 1 or 4°C for 7 days followed by 2 days at 24°C

N Respiration (CO2 production, mg Pyruvate content (FW basis,Electrolyte leakage (%)Varietya

kg−1 h−1) nmol g−1)

1°C 4°C 1°C 4°C 1°C 4°C

375 c3 *541 b9.0 ijK32b 17.1 gh56.1 cdefg73.8 bcde

67.3 bcdeK114 39.0 efg3 30.6 b * 10.9 gh 301 l 209 jHLGV 443 b550 ab15.2 e20.8 f72.4 bc80.8 bc3

425 de9.3 hij16.7 h 304 f62.8 bcdef104.6 a3MU64.6 bcde 48.3 cdefg 8.1 j + 30.6 a 236 m +E 325 e3

A 3 55.9 defg 320 e62.9 bcdef 12.7 i 8.4 j 440 d103.8 a 63.5 bcdeK 470 a568 a14.7 ef*3 29.0 bc

45.5 cdefg 17.8 gh 11.1 g44.6 fg 338 kT2 + 283 f362.5 bcdef 61.1 cdefg 19.8 fg 13.2 f 370 hij *3 228 INS×MU

3 41.4 g 34.6 g 28.0 bcd 19.1 d 377 ghi 279 fgE×HLGV239 I365 ij14.1 e19.8 fgH×K32 53.3 cdefg68.0 bcde3

74.7 bcd 68.9 bcd 36.8 a * 13.1 f 388 fghiT2×HLGV 271 g3396 fg21.0 bc26.7 cde59.5 cdefg65.7 bcde3HKC×HLGV 281 fg

235 I3A×HLGV 78.4 b 65.7 bcde 17.1 gh 10.5 ghi 321 klMU×NS 42.8 defg 24.3 e * 9.4 hij 322 kl 234 I67.1 bcde3

66.3 bcde 57.3 cdefg 12.7 iK114×H 8.2 j3 345 jk 254 h104.7 a 89.3 ab 35.2 aMU×K *3 22.2 b 375 ghi 270 g

HLGV×HKC 3 75.3 bcd 52.7 cdefg 17.4 gh 13.1 f 393 fgh 274 fg255 h3 105.4 a 102.7 a 25.3 e * 8.5 j 436 d *HLGV×T2

+434 d10.7 ghi*25.1 e 370 c65.0 bcde76.0 bc3K32×H57.9 cdefg 38.9 efgP76 11.5 i3 8.3 j 403 ef 280 fg

3 54.6 efg 35.6 fg 25.1 eM76 19.8 cd 504 c * 337 d

Mean 21.758.172.466 29740113.6LSD (0.05) 2.7527.848.620.0 11.413225.51.7811.35

a K32, Kecskemeti 32 and K114, Kecskemeti 114 (Hungary); HLGV, Hollandse Lange Groeme VO (Netherlands); MU,Monastyrski, Ulrich (Poland); E, Esvier and A, Amato (Netherlands), Kirak (Pakistan); T2, T2 (Netherlands); NS, Nochowski,Szklarniowy (Poland); HKC, Hybrid KC 291 (Netherlands); H, 2700817 (Hungary); P76, Poinsett 76; M76, Marketmore 76.

b Means followed by the same letter are not significantly different according to Fisher’s least-squares difference (LSD) (P=0.05).* and + denote significant differences between the two temperatures, where * is greater than the mean difference, while + is smallerthan the mean difference.


amined. However, in all cases, injury was moresevere after storage at 1°C than after storage at4°C. Chilling injury of sensitive plant tissues hasbeen characterized by the development of severalvisible symptoms and physiological dysfunctions,and for years, plant scientists have sought a uni-versal mechanism to explain all of the symptomsand dysfunctions observed. From the results ofthis study, it appears that low temperatures donot affect all biochemical and physiological pro-cesses of cucumber germplasm in the same way.Thus, correlations among various symptoms anddysfunctions in many cases are weak and pointto the importance of using more than one mea-sure in determining the susceptibility or resis-tance of a particular plant tissue to chillinginjury.

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