Does ethylene degreening affect internal quality of citrus fruit?

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  • Postharvest Biology and Technology 62 (2011) 5058

    Contents lists available at ScienceDirect

    Postharvest Biology and Technology

    journa l homepage: www.e lsev ier .com/ l

    Does e ty

    Lina May Poa Department o 50250b Vegetable and ty, Co

    a r t i c l

    Article history:Received 14 MAccepted 16 A

    Keywords:CitrusDegreeningEthyleneFlavorNutritional qu

    ver, eted pon ofnternethyleel orabreaeningnts adegrebility

    partially, to storage of the fruit for 5 days at 20 C. Nevertheless, ethylene degreening did not enhanceoff-avor perception or accumulation of off-avor volatiles, nor had any effect on levels of health pro-moting compounds such as vitamin C, total phenols and avonoids, or antioxidant-activity of citrus juice.We conclude that although ethylene affects peel color break, it is probably not involved in regulation ofinternal ripening processes in citrus fruit and, therefore, does not impair internal fruit quality.

    2011 Elsevier B.V. All rights reserved.

    1. Introdu

    In climaphysiologicing, includiacids, aromGiovanoni,their naturand ethylenexogenousrelated propigments anpeel tissueand Barmothese obserfruit to eth2030 C wand to rendNewhall, 19ing treatme

    CorresponE-mail add

    0925-5214/$ doi:10.1016/j.ction

    cteric fruit, ethylene plays a key role in governingal and biochemical changes that occur during ripen-ng color break, softening, and accumulation of sugars,a volatiles, vitamins, etc. (Lelievre et al., 1997; Barry and2007). In contrast, citrus fruit are non-climacteric, i.e.,al ripening is not accompanied by rises in respiratione production rates (Eaks, 1970). However, exposure toethylene has been shown to stimulate various ripening-cesses, such as destruction of the green chlorophylld accumulation of orange/yellow carotenoids, in citrus(Stewart and Wheaton, 1972; Barmore, 1975; Purvisre, 1981; Rodrigo and Zacarias, 2007). In the light ofvations, degreening practices involving exposure of theylene at concentrations of 25L L1 for about 72h atere developed, in order to accelerate peel color changeer the fruitmore acceptable formarketing (Grierson and60; Cohen, 1978). In particular, commercial degreen-nts are especially important for early varieties, in order

    ding author. Tel.: +972 3 9683617; fax: +972 3 9683622.ress: (R. Porat).

    to extend their marketing seasons, and for fruit grown in warm,tropical climates, such as those in Florida or India, where natu-ral color development is relatively weak (Wardowsky et al., 2006;Porat, 2008).

    Nevertheless, despite widespread knowledge of the effect ofethylene on peel color development, it is not yet known whetherexogenous ethylene regulates other biochemical changes associ-ated with internal ripening of citrus fruit, as it does in climactericfruit (Goldschmidt, 1998). The commondogma is that, in contrast toits effects on peel color change, ethylene has only relatively minoreffects on ripening processes in citrus esh, but this has neveryet been examined systematically. On the contrary, several linesof evidence suggest that ethylene may regulate various processesrelated to internal ripening. First, it is well known that exposureto ethylene accelerates respiration and ethylene-production ratesof citrus fruit, and these rates are indicators of activation of bio-chemical changes, such as breakdownof sugars and acids that serveas respiratory substrates (Aharoni, 1968; Vines et al., 1968; Eaks,1970). Second, previous studies have shown that ethylenedegreen-ing affects variousmetabolic pathways in citrus esh. For example,ethylene degreening decreased acidity levels in Mosambi oranges(LadaniyaandSingh, 2001), increasedproductionof aromavolatilesin green lemons (Norman and Craft, 1968), and slightly affectedaccumulation and composition of carotenoid pigments in the esh

    see front matter 2011 Elsevier B.V. All rights reserved.postharvbio.2011.04.005thylene degreening affect internal quali

    uonia, Zipora Tietela, Bhimanagouda S. Patil b, Ronf Postharvest Science of Fresh Produce, ARO, the Volcani Center, P.O. Box 6, Bet-DaganFruit Improvement Center, Department of Horticultural Sciences, Texas A&M Universi

    e i n f o

    arch 2011pril 2011


    a b s t r a c t

    Citrus fruit are non-climacteric. Howeing, stimulates various ripening-relachlorophyll pigments and accumulatiwhether exogenous ethylene affects iwe examined the possible effects ofof various citrus fruit, including Navsure to ethylene enhanced peel colorfruit tested. However, ethylene degreand had only minor effects on conteanalysis tests revealed that ethylenemarginally impaired sensory acceptaocate /postharvbio

    of citrus fruit?


    , Israelllege Station, TX 77845, USA

    xposure to exogenous ethylene, e.g., during ethylene degreen-rocesses in the peel tissue, such as destruction of the greenorange/yellow carotenoids. Nonetheless, it is not yet knownal ripening processes in citrus esh. To address this question,ne on taste, aroma, perceived avor, and nutritional qualitynges, Star Ruby grapefruit and Satsuma mandarins. Expo-k, and respiration and ethylene production rates in all citrushad no effect on juice total soluble solids and acid contents,

    nd composition of juice aroma volatiles. Moreover, sensoryening did not affect the avor of oranges and grapefruit, butof mandarins; the latter change could be attributed, at least

  • L. Mayuoni et al. / Postharvest Biology and Technology 62 (2011) 5058 51

    of Satsuma mandarins (Matsumoto et al., 2009). Third, it has beenreported that presence of ethylene in storage rooms results inloss of desired avor, and enhanced accumulation of off-avorsin oranges, whereas removal of ethylene from storage roomsimproves oet al., 1992)of 661 transfactor of at48h,whichmetabolic a

    In summvisual appeious adversit increasesand acceler1985; Carvaon whetheinuenced bestimated d

    Over theglobal martional beneare attachinquality of forder to evregulation ocitrus fruit,degreeningvor, and nuRuby grapethat ethyleripening prfruit quality

    2. Materia

    2.1. Plant m

    Navel ofruit (Citruscv. Miho)wSeptembersons. In allcolor breakthe packingvarietiesweMama.

    2.2. Ethylen

    Fruit weinto two lotlene for 24,them in 250amounts oftration of 4chromatogrushed dailnot exceedat 20 C, bu

    2.3. Juice socontents

    Total solwith aMod

    aciditypercentagesweremeasuredby titration topH8.3with0.1MNaOH by means of a Model CH-9101 automatic titrator (Metrohm,Herisau, Switzerland). Each measurement comprised ve replica-tions, eachusing juice collected fromthreedifferent fruit, i.e., a total

    ruit porbicby tmi eringcorbsed a


    it senexponts weatmferenof10t assnstrry stanceof rere

    f 15nsorre mrins


    ma ving tendebit eglassilutels wma v, eacher timupleere ancubes wexlbenzco, Bls hin atlo Al5mogran1,temLm

    or (Aat 7.7ctronc peaompologyof

    nearverall fruit quality (McGlasson and Eaks, 1972; Testoni. Fourth, we recently found that the expression patternscripts in mandarin esh were signicantly altered by aleast 3, following exposure to ethylene at 4L L1 forsuggests that this exposuremight have affected variousnd adaptation processes (Mayuoni et al., 2011).ary, notwithstanding its advantages in improving fruitarance, the ethylene degreening process also has var-e effects on fruit quality and postharvest storability:susceptibility to stem-end rots, enhances weight loss,ates rind and calyx senescence (Barmore and Brown,lho et al., 2008; Porat, 2008). Therefore, the decision

    r or not to degreen citrus fruit is not simple, and isy various circumstances, such as market demands andurations of storage and shelf life (Pool and Gray, 2002).last few years, because of increased competition in

    kets and increasing public awareness of the nutri-ts of horticultural produce, growers and consumersg increasing importance to the avor and nutritional

    ruit and vegetables (Kader, 2008; Patil et al., 2009). Inaluate the possible effects of ethylene degreening onf the internal ripening processes and on the quality ofwehave systematically examined theeffectsof ethyleneon taste, composition of aroma volatiles, perceived a-tritional quality of the citrus fruit Navel oranges, Starfruit, and Satsuma mandarins. Overall, we concludene is probably not involved in regulation of internalocesses in citrus and, therefore does not impair internal.

    ls and methods


    ranges (Citrus sinensis [L]. Osbeck), Star Ruby grape-paradisi Macf.), and Satsuma mandarins (Citrus unshiuere purchased fromcommercial packinghouses during

    through November of the 2009 and 2010 growing sea-cases, fruit were harvested at the beginning of natural, and were collected directly from the harvest bins athouse. For taste score evaluations, additional mandarinre also tested, including Michal, Odem, Or, Mor, and

    e degreening

    re selected for uniformity of size and color, and divideds, which were exposed, respectively, to air or to ethy-48, or 72h. They were exposed to ethylene by placing-L airtight sealed plastic tanks, into which appropriatepure ethylene were injected, to achieve a nal concen-L L1. Ethylene concentrations were veried by gasaphy according to Porat et al. (1999). The tanks werey to ensure that accumulated carbon dioxide levels did0.2%. Control fruit were held in the same storage roomt without ethylene.

    luble solids, titratable acidity, and ascorbic acid

    uble solids (TSS) content in the juice was determinedel PAL-1 digital refractometer (Atago, Tokyo, Japan), and

    of 15 fAsc

    minedto Hirocompa0.1% asexpres

    2.4. Se

    FrudaysofsegmeEach trve difsistingpanelisto an uand veas distmeanselists wscale oThe sehere amanda

    2.5. An

    Aroaccordand blto inhi10mLMO), dThe via

    Aromentsfruit p(GC) copleswwere iVolatilStable-diviny(Supelthe viafor 5mlent, PaID, 0.2was pr5 Cmiat thatat 0.8mdetectto 206the elegraphieach cTechnocationtheir lier measurement.acid (vitamin C) contents in citrus juice were deter-

    itration with 2,6-dichlorophenolindophenol accordingt al. (1980). Ascorbic acid levels were determined bythe titration volumes of citrus juices with those ofic acid (SigmaAldrich, St. Louis, MO), and results ares milligrams of ascorbic acid per 100mL of juice.

    y evaluations

    sory qualitywas tested on the day of harvest and after 5sure toair or ethylene. Fruitwerepeeled, and separatedere cut into halves and placed into covered glass cups.ent included a mixture of cut segments prepared fromt fruit. Fruit tastewas evaluated by a trained panel con-members,vemalesandve females, aged2562.Eachessed the various attributes of three samples, accordinguctured 100-mm scale, with anchor points very weakrong for each attribute, and sensory datawere recordeds (mm) from the origin. The samples were identied byandomly assigned three-digit codes. In addition, pan-requested to rate overall fruit avor preference on a: 1 =very bad, 2 =bad, 3 = fair, 4 = good, and5=excellent.y analysis scores of oranges and grapefruit presentedeans of three independent experiments, and those ofare means of six independent experiments.

    is of aroma volatiles

    olatiles were extracted from homogenized segmentso Tietel et al. (2010a). Fruit were hand-peeled, weighed,d for 30 s with an equal amount of 30% NaCl (w/v),nzymatic degradation. Aliquots (2mL) were placed invials, and 5L of 1-pentanol (SigmaAldrich, St. Louis,d 1:1000 in water, were added as an internal standard.ere stored at 20 C pending analysis.olatiles were determined by three replicate measure-prepared from three different fruit, i.e., a total of ninee point. They were identied by gas chromatographyd with mass spectrometry (MS). Prior to analysis, sam-llowed to equilibrate for 5min at 40 C, afterwhich theyated at the same temperature for an additional 25min.ere extracted by solid-phase microextraction (SPME).bers, 1 cm in length, coated with a 50/30m layer ofene/carboxen/polydimethylsiloxane (DVB/CAR/PDMS)ellefonte, PA) were used to trap volatile compounds ineadspaces. After incubation, the bers were desorbed250 C in the splitless inlet of a Model 7890A GC (Agi-to, CA) equippedwith anHP-5 column (30m0.25mmlm thickness) (J&W Scientic, Folsom, CA). The oven

    mmed to run at 50 C for 1min, to ramp up to 160 C atthen to ramp up to 260 C at 20 Cmin1, and to remainperature for 4min. The helium carrier-gas ow was setin1. The efuent was transferred to a Model 5975CMSgilent, Palo Alto, CA) that was set to scan from mass 402 scans/s, in the positive-ionmode, andmass spectra inimpact (EI) mode were generated at 70eV. Chromato-ks were identied by comparing the mass spectrum ofnent with the US National Institute of Standards and(NIST) library of mass spectra, 2006 version. Identi-

    aroma volatiles was further conrmed by calculatingretention indices (RIs) by comparison with a series of

  • 52 L. Mayuoni et al. / Postharvest Biology and Technology 62 (2011) 5058

    Fig. 1. Visual

    n-alkanes (Cdatabases orus Flavor Dof interestinternal staThe identitmethylbuta-terpinene4-ol werestandards.

    2.6. Determ

    Phenolssamples wappearance of Navel oranges, Star Ruby grapefruit and Satsuma mandarins at harvest

    5C20) and comparing their values with the publishedf Adams (2001) and the University of Florida Cit-atabase ( Peakswere semi-quantied by comparison with added

    ndards, and are expressed as 1-pentanol equivalents.ies of 11 compounds, including -pinene, ethyl 2-noate, hexanal, -myrcene, -terpinene, limonene,, octyl acetate (E)-2-nonenal, linalool, and 1-terpinen-further conrmed by running authentic chemical

    ination of total phenols and avonoids

    and avonoids were extracted by stirring 1mL juiceith 9mL of 80% methanol for 30min at room tem-

    perature, fTotal pheno(Singleton0.2mLof juand 7mL of90minat romeasuredaphenolic co

    Total aBriey, theextracts, 0.3mixtures w1N NaOH wwas adjustecontents wand after 24, 48 and 72h of exposure to ethylene at 4L L1 at 20 C.

    ollowed by centrifugation at 10,000 g for 10min.lics were determined by the FolinCiocalteu method

    et al., 1999). Briey, the reaction mixtures comprisedicemethanol extracts, 0.2mLof FolinCiocalteu reagent,7% Na2CO3. The reaction mixtures were incubated foromtemperature, afterwhich absorbance at 750nmwasgainst apreparedblankwitha spectrophotometer. Totalntents were expressed as gallic acid equivalent (GAE).vonoidsweredeterminedaccording to Shin et al. (2007).reaction mixtures comprised 1.0mL of juice methanolmL of 5% NaNO2 and 0.3mL of 10% AlCl3. The reaction

    ere incubated for 10min at room temperature, 2mL ofere added to stop the reaction, and the total volumed to 10mL by adding double-distilled water. Flavonoidere measured by comparing the absorbance at 510nm

  • L. Mayuoni et al. / Postharvest Biology and Technology 62 (2011) 5058 53

    Fig. 2. Evaluatto air or to eth

    with that ofequivalent

    2.7. Antioxi

    Total anradical catimixture coazinobis-(3solved in areactionmiAfterwardswith that ofthe degreeabsorbanceEquivalent(mM)= (Absresults werity (TEAC), cV= sample v

    2.8. Statisti

    One-waywise compstatistical sMicrosoft Oion of respiration and ethylene production rates of Navel oranges, Star Ruby grapefruitylene at 4L L1 at 20 C. Data are means SE of six replications...


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