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PHYSIOLOGICAL CONSEQUENCES OF MINIMALLY
PROCESSED FRUITS AND VEGETABLES

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ROSA S. ROLLE and GRADY W.CHISM LU'
Department of Food Science and Nutrition
lhe Ohio Agricdtund Research and Dcvelopmnt Center
The Ohio State University
Columbus, Ohio 43210

Accepted for Publication June 26, 1987

ABSTRACT
l'he physiological consequences of minimal processing are dire. Mechanical
injury sets offa complex series of events which result in loss of quality (i.e. col-
or, texture and fiver). Control of this wounding response is a tnqjor obstacle
that must be overcome. To prolong postharvest life, respiration must be reduced
while producing enough energy to maintain the "energizedstate". 'Ihe central
roles of membranes and calcium in maintaining quality are discussed.

INTRODUCTION
For the purposes of this review, we define minimal processing to include all of
the unit operations (washing, sorting, peeling, slicing, etc.) that might be used

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prior to blanching in a conventional processing line. Thus, minimaUy processed

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tissues have been exposed to substantial injury due to cutting. Minimally pro-
cessed fruits and vegetables differ from conventionally p m s s e d tissues
because they have not been blanched and therefore are still living respiring
tissues.
The number one priority of all living tissues is to maintain the "energized
state. Once detached from the parent plant, energy must be supplied by utiliz-
ing stored carbohydrate, lipid or protein. Respiration, the conversion of these
stores of energy, is essential in order to maintain the "energized state. If I'

respiration cannot supply enough energy to maintain the "energized state ",then
the tissues will rapidly deteriorate and die. This deterioration leading to cellular
death begins in the membranes which must be maintained if the cells are to func-
tion normally. Practical experience has demonstrated that tissues having large
energy reserves generally have longer postharvest lives. Controlling respiration
*&nd correspondence to: Grady W.Chism, III. Dcpt. Food Science & Nutrition, The Ohio State
University, 122 VH-2121 Fyffe Road. Columbus, Ohio 43210.
Journal of Food Quality 10 (1987) 157-177. All Rights Reserved.
QCopyrighr 1987 by Food & Nutrition Press, Inc., Wespon, Connecricut. 157
158 zyxw
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ROSA S. ROLLE AND GRADY W.CHlSM IIl

so that the "energized state" is maintained with a minimal depletion of energy

reserves increases postharvest shelf-life. This is generally accomplished for
fruits and vegetables via either low temperature or modified atmosphere storage.
The second major obstacle to be faced in minimally processed fruits and
vegetables is that of mechanical injury or wounding. The response to wounding
sets into motion a complex series of events designed to repair the damage. Many
of these events are deleterious to quality, and control of wounding and/or the
consequences of it are a major challenge to the postharvest life of minimally pro-
cessed fruits and vegetables.

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Consequences of Environmental Factors used to Control Respiration

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Low Temperature Storage. Respiratory patterns of fruits and vegetables in
response to low temperatures arc variable. Those which are tolerant of low
temperatures show a decrease in respiration rate with a decrease in temperature,
and maintain their respiratory activity in balance with glycolysis at low
temperatures (Lyons er al. 1979). Many chilling sensitive fruits and vegetables
on the other hand show increased respiratory rates at chilling temperatures (Eaks
and Moms 1956; Lewis and Moms 1956; Eaks 1960), presumably due to un-
coupling of oxidative phosphorylation (Eaks 1960; Creencia and Bramlage
1971). Lyons (1973) suggested that the increased respiration observed must
reflect an injury phenomenon which upsets metabolism.
When subjected to temperatures of less than 12.5 "Cbut higher than freezing,
most horticultural crops undergo physiological injury (Chaplin er al. 1982;
Couey 1982; Van Lelyveld and Bower 1984; Purvis 1984; Vazquez-Salinas and
Lakshminarayana 1985; Morris 1982). The injury sustained under such condi-
tions is termed "chilling injury " since freezing is not involved.
The impairment of membrane function is most likely the major contributing
factor during storage at temperatures which induce chilling injury (Hultin 1981).
Lyons (1973). suggested that chill injury results from changes in the configura-
tion of the cellular membrane (from a liquid crystalline to a gel state) occuring at
the critical temperature for the Occurence of chilling injury: Uritani (1978) and
Raison and Wright (1983) postulated that the susceptibility of chilling sensitive
plants was related to the lipid components of the membranes, in particular the
phospholipids.
Markhart (1986), noted that a change in state brought about by chilling injury,
decreases membrane permeability and changes the activity of membrane-
associated enzymes and enzyme systems which results in major alterations in
metabolism. According to Lyons (1973) and McGlasson and Raison (1973),
changes in the membrane on chilling lead to modification of the activity of mem-
brane bound enzymes, to alterations in membrane permeability and thus altered
metabolism. Disruption of mitochondrial function inhibits membrane bound en-
zymes such as those of the TCA cycle while not affecting glycolytic enzymes of
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PHYSIOLOGICAL CONSEQUENCES

the cytoplasm, thereby creating an imbalance of the pathways involved. The net
effect of this imbalance is the accumulation of glycolytic products such as
acetaldehyde, pyruvate and oxaloacetate which are potentially toxic to the cell
and impart off flavors.
The accumulation of pyruvate (Murata 1%9), acetaldehyde (Murata 1969;
Davis er af. 1974; Eaks 1980), ethanol (Murata 1969; Davis et af. 1974, Eaks
159

1980) and a-keto acids (Murata 1969) in chilled fruit tissues has been reported.
Roof of the toxicities of these compounds at physiological concentrations has
not however been absolutely established.
Recently Wise and Naylor (1985, 1987a, 1987b) presented data which sug-
gested that the mechanism of chill-induced injury was due to lipid peroxidation.
They suggested that superoxides may be involved in generating injury, and that
naturally occuring antioxidants may serve as protectors against this injury.
Ethylene production in a number of plants is stimulated by chilling
temperatures (Wang er af. 1971; Sfakiotakis and Dilley 1974; Ichii and Hamada
1978; Wang and Adams 1980). The pathway for ethylene biosynthesis in chilled
tissues is the same as that in ripening fruits (Wang and Adams 1980). Increased
ethylene production in chilled tissues is due to increased capacity of the tissue to
synthesize 1-aminocyclopropane-1carboxylic acid, (ACC). Enzymatic activity
associated with conversion of ACC to ethylene, mediated by ethylene forming
enzyme, EFE, is however apparently damaged by chilling temperatures (Wang
and Adams 1980). Ethylene adversely affects the color of green vegetables
under chilling conditions (Pendergrass et af. 1976; Toivonen er al. 1982).
Prechilling ethylene treatment of some fruits and vegetables has been shown to
reduce chilling injury (Lipton and Ahroni 1979; Lipton and Mackley 1985; Lip-
ton and Wang 1987) and ACC accumulation (Lipton and Wang 1987). Whether
accelerated ethylene production in chilled tissues is related to physical transi-
tions of the membrane is still unknown (Wang 1982).
Symptons of chilling injury involve necrosis of groups of cells at the surface

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and within the tissues. Death of these cells leads to internal browning, external
discoloration, surface pitting and thus increased susceptibility to infection all of
which adversly affect quality. The severity of symptoms manifested is dependent
on the storage temperature (Lipton 1978; Wade 1979; Moms 1982; McDonald
et al. 1985). As storage temperature of the produce decreases below the critical
threshold temperature, the severity of ultimate injury increases though the rate of
development of injury during cool storage is decreased (Wade 1979). A
simplified scheme of the biochemical responses of plants to chilling stress was
presented by Wang (1982).
Approaches to alleviation of chill injury have been thoroughly reviewed by
Wang (1982). They include temperature conditioning (Hatton and Cubbedge
1982; Hatton and Cubbedge 1983; Chalutz er af. 1985; Pichia 1984; Pichia
1986), intermittent warming of produce (Davis and Hofmann 1973; liker and
160 zyxw
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zyx ROSA S.ROLLE AND GRADY W. CHISM IIl

Moms 1975; Wang and Baker 1979; Wade 1979; McDonald et af. 1985) and
controlled humidity storage. High humidity is thought to reduce desiccation of

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necrotic tissues thereby suppressing the symptomsof injury (Lyons 1973), while
low humidity is thought to enhance loss of volatile esters of compounds which
are of low or suspected toxicity.
Controlled Atmosphere Storage. Where low temperature storage of fruits
and vegetables is not feasible, the use of low oxygen (1-3% 0,) and high carbon
dioxide (5-2076 C02) levels as a means of controlling their environment and
thus influencing their respiration and shelf-life are exploited.
A minimum of 1-3% O2 depending on the commodity, i s necessary for
maintenance or aerobic respiration. O2 concentrations of less than 1% create
anaerobic conditions in the cells, whereby energy requirements of tissues are
supplied via glycolysis rather than through the TCA cycle. Glycolytic products
build up and lead to off flavor development.
High COz levels may delay ripening and extend storage life. High COz con-
centrations decrease energy supplies to tissues by inhibiting various respiratory
enzymes (Bendall et a1 1960; Miller and Evans 1956; Shipway and Bramlage
1973; Walker and Brown 1957) and uncoupling oxidative phosphorylation
(Fanestil er al. 1963). Jingtair and Kader (1986) observed reduced glucosed-
phosphate levels in lettuce under C02treatment, and suggested that this was due
to enhancement of glycolysis, indicating a need for energy supply by tissues to
sustain an adequate energy status under such conditions. However, the mode of
action of CO, in respiratory metabolism is still unclear.
Elevated CO, concentrations do not always produce desirable effects. They
inhibit succinic dehydrogenase activity whch results in accumulation of succinic
acid, a toxicant to plant tissues (Bendall et al. 1960; Williams and Patterson
1964; Monning 1983). Further, they may bring about pH changes within the
tissue leading to a point where normal physiological function is no longer sus-
tainable (Jingtair and Kader 1986).
Storage of h i t s and vegetables under controlled atmosphere conditions has
differential effects on various quality attributes. Low O2levels have been shown
to delay chlorophyll loss in tomatoes (Goodenough and Thomas 1980) and ap-
ples (Knee 1980), and to retard the rate of flesh softening in apples (Knee 1980).
Such conditions however promote off-flavor development in broccoli(Kasmire et
01. 1974) and adversely affect wound healing of bruised potatoes (Wiggington
1974; Lipton 1975).
Ethylene production by ripening fruit is an oxygendependent process. Levels
of 0,less than 8% decrease ethylene production by fruits and vegetables (Burg
and Burg 1967; Burg and Burg 1969; Lau etaf. 1984; Yoshida etal. 1986). This
is due to inhibition of conversion of ACC to ethylene within the tissues since
steps in ethylene biospthesis from methionine occur in the absence of 0,(Yang
1985). Ethylene-induced physiological disorders have been shown to be
alleviated by low O2 concentrations (Kader 1985).
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PHYSIOLOGICAL CONSEQUENCES 161

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Elevated COz levels on the other hand have differential effects on ethylene
production rates by fruit, depending on the commodity and the COz concentra-
tion. Elevated COz levels may reduce (Kader 1985) or aggravate (Arpaia er d .
1985; Arpaia er al. 1986) ethylene induced physiological disorders.
Some reactions are beneficially influenced by elevated C02 levels, while
others are adversely affected by it. Elevated COz levels delay brown discolora-
tion of lettuce (Siriphanic and Kader 1985) and mechanically damaged green
beans (Buescher and Henderson 1977) by inhibiting formation of phenolic com-
pounds and phenolase activity, while they enhance the undesirable brown

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discoloration of grapes (Nassar 1966; Yahia et al. 1983) and mushrooms ( M u

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and Moms 1974).
Desirable textural effects promoted by elevated COz levels include retarded
toughening of asparagus spears (Lipton 1975) and tenderization of broccoli (Lip-
ton and Harris 1974). The pathologicalbreakdown of strawberries(El-Kazzaz et
d . 1983a), blackberries (Momset af. 1981) and bluebcmes (Ceponis and Cap-
pellini 1985) is suppressed by elevated COz.

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Consequences of Mechanical Iqjury
Mechanical wounding may induce a diverse array of metabolic pathways and
hence bring about changes in metabolism. These changes include localized in-
creased respiration at the site of injury, stress ethylene production, accumulation
of secondary metabolites, and cellular disruption leading to decompartmentation
of enzymes and substrates. These responses are brought about subsequent to a
series of reactions designed to bring about membrane restoration in plant tissues,
The membranes of plant cells and of subcellular organelles are lipoprotein
structures in which the lipid components are predominantly phospholipids and
galactolipids (Galliard 1978). Wounding or injury damages membrane systems
of cells (Bangerth 1979; Mazliak 1983; Simmons er af. 1984) causing membrane
components to undergo extensive enzymatic degradation (Kemp ct al. 1974;
Galliard and Phillips 1976; Galliard er al. 1976; Galliard and Matthew 1976;
Wardale er al. 1978; Feys et al. 1980; Yapa et d.1986), and to be depleted of
their lipid components. Loss of compartmentation of enzymes and substrates
within the cells ensues.
Loss of membrane lipid components is mediated by the action of lipid acyl
hydrolases (Galliard 1968; Galliard 1971; Galliard 1975; Wardale and Galliard
1975; Wardale and Galliard 1977) and phospholipase D activity (Galliard 1979;
Yapa et al. 1986) and results in the production of fatty acids. The fatty acids
liberated are capable of disrupting biological systems causing lysis of organelles,
and binding to and inactivating proteins (Galliard 1979). They are substrates for
further enzymatic activity and are activated via either of two routes: a-oxidation
(Galliard and Matthew 1976; Laites et af. 1972) or lipoxygenase activity
(Galliard and Phillips 1976). Volatile long chain aldehydes are produced during
a-oxidation of fatty acids in disrupted cucumber fruit (Galliard and Matthew
162 zyxw
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1976) and are responsible for "wound respiration " induced by cutting through

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potato tissues (Laites and Hoelle 1967).
Lipoxygenase activity catalyzes the peroxidation of polyunsaturated fatty
acids with a cis, cis 1,4 pentadiene structure to form conjugated hydroperoxides
which are converted to a variety of carbonyl compounds and oxygenated
derivatives. Free radicals arc generated as by-products of this activity (Verhagen
et al. 1978) and can cause leakiness in membranes and release of stored
hydrolytic enzymes and organic acids from the vacuole, thus accentuating
damage (Omarkhayyan 1986). Free radicals are also capable of attacking the
protein moiety of the membrane contributing to further membrane disintegra-
tion. This activity may be somewhat arrested by the presence of naturally occur-
ing antioxidants within the membrane lipid bilayer (Mead 1976).
A series of additional side reactions occur concurrent with these activities in
order to facilitate continuation of respiratory processes. Steps of the electron
transport chain which were inhibited in intact tissues are unblocked (Laites
1963) and the TCA cycle is unblocked due to destruction of the inhibitor

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7-hydroxy-ketoglutarate (Laites 1978). Thus throughout wound healing,
respiration ("induced respiration") is fed through enhanced breakdown of
starch, accelerated catabolism of sugars via glycolysisas well as activation of the
TCA cycle (Kahl 1983). These processes cater for the regeneration of ATP.
Wound-induced changes in the membrane cause release of ethylene ( "wound
ethylene") (Mattoo and Liebermann 1977; Mattoo et al. 1979; Hyodo et al.
1984; Mattoo and Anderson 1984). Yang and Pratt (1978) concluded that the
biosynthetic pathway for ethylene under such conditions is similar to the
pathway for ethylene synthesis in ripening fruit. ACC synthase shows increased
activity in tissues following wounding (Roller et al. 1979; Boller and Kende
1980; Yu and Yang 1980; Mattoo et al. 1983, Hyodo et al. 1985) and may be
synthesized de novo in wounded tissue (Acaster and Kende 1983; Hyodo et al.
1983). Increased ACC synthase activity following wounding causes accumula-
tion of ACC and thus the onset of "wound ethylene 'production (Yu and Yang
1979; Hyodo er o f . 1985).
Mattoo and Anderson (1984), presented a model showing possible sites for
control of the ethylene biosynthetic pathway in wounded tissues. According to
these authors, membrane associated ACC may interact with membrane-bound

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ethylene forming enzyme (EFE). During this interaction, ACC produced by
ACC synthase is synthesized in close proximity of the EFE which uses ACC to
produce ethylene. Roles for "wound ethylene " in wound healing, phytoalexin
production and increased disease resistance have been suggested, however, the
physiological role of wound ethylene is unknown, and its full consequences on
quality are not understood (Haard 1985).
Physiological changes discussed thus far are geared toward the ultimate seal-
ing of the injury and wound healing in the tissues. The wound response of the
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PHYSIOLOGICAL CONSEQUENCES 163

tissues is dependent on the tissue concerned, and the trauma to which it is sub-
jected. a-solamarine, P-solamarine, a-solanine and achaconine which have
bacteriostatic and fungistatic properties accumulate in potato tuber slices (Kahl
1974), while suberin, a protective tissue is deposited on woundcxposed cell
walls of potato tissues (Kolattukudy 1978), tomato fruit and bean pods (Dean

metabolite (Haard and Cody 1978).

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and Kolattukudy 1976). In potatoes, /3-solamarine is the principle stress
metabolite produced in response to cut injury under dark storage conditions,

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while in the presence of U.V. radiation, a-solanine is the principle stress

A host of metabolites which affect food color, texture and flavor are generated
by the metabolic changes accompanying wounding. In fact, the browning induc-
ed by wounding may be one of the limiting factors for minimally processed fruits
and vegetables. Wounding induces phenylalanine ammonia lyase (Hyodo et al.
1978;Hanson and Havir 1979),polyphenol oxidase (Mason 1955;Kahn 1977;
Bower and Van Lelyveld 1985)and a number of other enzymes which contribute

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directly or indirectly to browning. Classically these reactions have been controll-
ed utilizing sulfite but regulatory and marketing constraints preclude the con-
tinued usage of this highly affective agent. Compounds formed in the wound

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healing process may adversely affect flavor (Chalutz et al. 1969; Sarkar and
Phar 1979),and texture (El Kazzaz et 01. 1983)and are generally of suspected or
known toxicity to humans (Scheel et al. 1%3; Jadhav and Salun khe 1975;Oku
et al. 1976).
The products of lipoxygenase activity are significant contributors to desirable
or off flavors in foods depending on their concentrations (Josephson et al. 1983).
Lipoxygenase activity is responsible for desirable flavor production in
cucumbers (Galliard et al. 1976a;Galliard et al. 1976b)and tomatoes (Galliard
and Matthew 1977).Grassy and beany flavors in soy products produced as a
result of cleavage of hydroperoxides into volatile aldehydes (Kalbrener et a f .
1974)are however, undesirable products of lipoxygenase activity.
Lipoxygenase activity catalyzes the co-oxidation of pigments (kens et al.
1973;Weber er al. 1974;Grosch 1976;Ikediobi and Snyder 1977), and has a
bleaching effect on carotenoids (Weber et al. 1974;Blain 1970;Klein et al.
1984), and chlorophyll (Imamura and Shimizu 1974;Holden 1974;Klein et al.
1984) which is deleterious to the postharvest quality of fruits and vegetables.
Further, lipoxygenase activity depletes nutritional value of food by degrading
essential fatty acids.
Ethylene promotes senescence and accelerated deterioration in harvested
crops (Kader 1985). The majority of color, flavor and textural changes brought
about in fruits and vegetables postharvest are either directly or indirectly af-
fected by ethylene. These changes were thoroughly reviewed by Kader (1985).
Wounding may cause water-loss from tissues which adversely affects the texture
and nutritional quality of produce.
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164 ROSA S.ROLLE AND GRADY W.CHISM III

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Comequences Related to Calcium
In recent literature, much attention has been focused on calcium because of the

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desirable effects it has on enhancing the quality of fruits and vegetables
postharvest (Faust and Shear 1972; Mason 1976; Bangerth 1979; Arteca et d.
1980; Collier and Tibbitts 1982; Hopfinger ct d.1984). Its desirable effects in
fruits and vegetables include reduced respiration (Banged er al. 1972; Bangerth
1973; Bramlage et al. 1974; Cooper and Banged 1976) delayed senescence
(Liebennann and Wang 1982; Poovaiah and Leopold 1973; Poovaiah 1979;
Suwwam and Poovaiah 1978) and increased firmness (Poovaiah 1986; Bangerth
et al. 1972).
Physiological disorders caused by inadequate calcium levels in fruit tissues
have also received much attention and are very well documented (Drake er al.
1974; Shear 1975; Sharples and Johnson 1976; Hopfinger and Poovaiah 1979;
Mullaway and Wiersholm 1979; Banged 1979; Cocucci et al. 1983; Conway
and Sams 1984). Increased calcium levels generally decrease the wcurence of
these disorders.
Calcium is essential to maintaining the structural integrity of membranes and
cell walls. Evidence for the role of calcium in membranes was summarized by

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Poovaiah (1986): (1) Calcium deficient conditions promote membrane deteriora-
tion (Marinos 1962; Yapa et al. 1986). (2) Calcium alters the architecture of
membranes; its introduction into membranes (Paliyath ct al. 1984; Zaho er al.
1987) results in enormous changes in fluidity and water permeability. (3)
Calcium can powerfully alter an array of physiological activities which are
associated with membrane function i.e., can turn on active transpon of some
ions through membranes (Hanson 1983) or increase conversion of ACC to
ethylene in tissues via stabilization of the plasma membrane (Liebermann and
Wang 1982; Legge et al. 1982).
Calcium plays a special role in maintaining the cell wall structure in fruits and
other storage organs by interacting with pectic acid in the cell walls to form
calcium pectate. Calcium is important in maintaining cell permeability and com-
partmentation. Most calcium deficiency disorders result in flesh browning,
brought about by increased leakage of phenolic precursors form the vacuole to
the cytoplasm with subsequent oxidation by phenolase enzymes. Wienke (1980)
suggested that calcium introduced into apples by postharvest treatment is incor-
porated into the cell wall in the same manner as native calcium.
Ethylene production is stimulated in calcium deficient tissues (Faust and Shear
1969; Liebermann and Wang 1982). However, addition of calcium to calcium
deficient tissues decreases respiration and suppresses ethylene production
(Poovaiah and Leopold 1973; Faust 1975; Liebermann and Wang 1982)
presumably due to a certain degree of oxidative metabolism (Frost 1986).
Calcium reduces respiration rates by limiting diffusion of substrate from the
vacuole to the respiratory enzymes in the cytoplasm (Bangerth er d. 1972).
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PHYSIOLOGICAL CONSEQUENCES

Liebermann and Wang (1982) suggested that the ethylene forming system
I65

resides in the plasma membrane which is preserved by calcium.

Various postharvest calcium treatment methods and the factors affecting
calcium uptake by tissues are beiig studied to increase the calcium content of
fruits and vegetables. The use of calcium for extension of postharvest shelf-life
certainly has great potential.

SUMMARY
The physiological consequences of minimal processing are dire. Mechanical
injury sets off a complex series of events which result in loss of quality (i.e. col-
or, texture, and flavor). Control of the wounding response is a m j o r hurdle for
extending the shelf-life of minimally processed plant tissues. The other major
obstacle is to maintain membrane integrity. Adequate energy must be provided
through respiration for this purpose. Calcium treatments may prove to be very
useful in controlling some of these responses but finding an adequate replace-
ment for sulfite in controlling browning is essential to expanding the use of
minimally processed fruits and vegetables.

ACKNOWLEDGMENTS
Presented at the meeting of The Southern Association of Agricultural Scien-
tists, Nashville, Tenn. Feb. 1987.
Salaries and research support provided by The Ohio Agricultural Research
and Development Center, The Ohio State University. Journal Article No.
137-87.

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PHYSIOLOGICAL CONSEQUENCES

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177

alteration of membrane permeability of Quercus rubru root cortez cells. Plant

Physiol. 83, 159-162.