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Chapter 37
Application of Polyamines to Maintain Functional
Properties in Stored Fruits
Marı́a Serrano and Daniel Valero
Abstract
Polyamines are natural compounds involved in many growth and developmental processes with ubiquitous
presence in all cells. Research in fruits has been developed to get a better understanding of the role of
polyamines, both endogenous and exogenous, especially during the ripening and senescence processes.
However, in recent years and given the relationship between fruit consumption and human health, the
study of antioxidant compounds responsible for these beneficial effects is of increasing interest.
This chapter focuses on the role of polyamines on the content of bioactive compounds with antioxidant
activity as well as in the activities of the main antioxidant enzymes in fruits.
Key words Postharvest, Putrescine, Spermidine, Spermine, Antioxidants, Phenolics, Anthocyanins,
Carotenoids, Antioxidant enzymes
1
Introduction
The polyamines have a long history, and the first evidence was
obtained in 1678 by Antonie van Leuwenhoek which described
the presence of crystalline substances in the human semen, but was
in 1878 when these crystals were identified as spermine by Laudenburg and Abel [1]. In 1924 putrescine (Put), spermidine (SPd),
and spermine (Spm) were synthesized [2]. During the midtwentieth century the experiments with polyamines were carried
out in bacteria while experiments with animals appeared in the
1970s with special interest in the association between polyamines
and diseases and largely focused on cancer cells leading to a synthesis of the inhibitor of polyamine synthesis DFMO (α-difluoromethylornithine). In plants, the first evidence to the occurrence
of Put was dated in 1911 but was in 1971 [3] when it was concluded that Put, Spd, and Spm are ubiquitous organic cations in
higher plants.
Polyamines are involved in many aspects of plant development
and considered as important molecules associated with both abiotic
Rubén Alcázar and Antonio F. Tiburcio (eds.), Polyamines: Methods and Protocols, Methods in Molecular Biology,
vol. 1694, DOI 10.1007/978-1-4939-7398-9_37, © Springer Science+Business Media LLC 2018
449
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Marı́a Serrano and Daniel Valero
and biotic stresses, the most studied in fruits being chilling injury
(CI). Thus, polyamines have been reported to stimulate cell division, dormancy breaking, germination, development of flower
buds, fruit set and growth [4–8]. However, one of the main aspects
of the relationship between polyamines and fruit are those related
to fruit ripening. Generally, there is an inverse relationship between
the content of endogenous polyamines and ethylene production
which is attributed to the fact that both share the common precursor S-adenosylmethionine (SAM) in their biosynthesis pathway [6].
This relationship has justified the large body of knowledge about
the application of polyamines, either at pre-harvest (during fruit
growth and ripening on tree) or after harvest (postharvest treatments) to delay the postharvest ripening process and maintain fruit
quality attributes such as colour, firmness, acidity, and total soluble
solids during postharvest storage, either at ambient temperature or
under cold storage [6, 9, 10]. However, the role of these treatments on the content of bioactive compounds and antioxidant
activity has been poorly studied. In this chapter we present the
recent literature about the effect of polyamines as pre- or postharvest treatments on the content of phytochemicals with antioxidant
properties in fruit, at harvest and during storage, given the health
beneficial effects attributed to these compounds.
2
Fruit and Health Beneficial Effects
Nowadays, it is widely accepted that nutrition has a great influence
on health and increasing evidence suggests that diets rich in fruits
and vegetables may prevent a wide range of diseases, mainly cardiovascular diseases (by reducing risk factors such as diabetes, hypertension, and hyperlipidemia, platelet aggregation, blood pressure,
insulin resistance index, and obesity), several kind of cancers, such
as colon, oesophagus, oral cavity, stomach, pancreas, prostatic,
breast, and ovary (by regulating gene expression in cell proliferation
and apoptosis), neurodegenerative diseases, brain and immune
dysfunction, and even against bacterial and viral diseases [11–13].
These effects are due to phytochemical compounds with antioxidant activity, the most important being phenolics, including anthocyanins, carotenoids, vitamins (C and E), and glucosinolates
[14–18]. In addition, it is important to note that whole fruit intake
provides more health beneficial effects than one of their constituent, because of additive and synergistic effects [13, 14].
Dietary polyamines from plant origin are considered very
important for human health. The body pool of polyamines in
human body is maintained by three sources: endogenous or de
novo biosynthesis, produced by the gut microbiota, and exogenous
intake through the diet [19]. From these sources, the polyamines
derived from the diet are the most important from the point of view
Application of Polyamines to Maintain Functional Properties in Stored Fruits
451
of quantity, since the capacity to synthetize polyamines decreases
with age. Some of the health-beneficial effects of dietary polyamines are those related to protection against oxidative stress, maintenance of gut integrity, modulation of inflammation and immune
functions, among others [20]. It seems that polyamine antioxidant
activity leads to reduction in both cell membranes and DNA [21].
The average intake of dietary polyamines is different depending
on the country. In Europe, the highest intake of total polyamines
(700 μmol per day) has been estimated in the Mediterranean
regions compared with northern Europe. This difference could
justify the protective role attributed to the Mediterranean diet.
Among the different food groups, fruit provides the highest
amount of Put (500 μmol/kg) while cheese contains over
600 μmol/kg of Spd [19–21].
3
3.1
Polyamines, Bioactive Compounds and Antioxidant Activity in Fruits
Carotenoids
Carotenoids are a group of natural-lipophilic pigments with a general structure of C40 tetraterpenoids responsible for yellow to red
colour in fruits. The carotenoids are classified as carotenes (ßcarotene, lycopene, etc.) and xanthophylls. In addition, carotenoids
can be acyclic (e.g. lycopene), monocyclic (γ-carotene), or dicyclic
(α- and ß-carotene). The most studied carotenoids have been ßcarotene, lycopene, lutein and zeaxanthin which exhibit a potent
antioxidant activity. The antioxidant ability of these carotenoids
(carotenes and xanthophylls) follows the sequence from high to
low: lycopene > ß-cryptoxanthin ß-carotene > lutein zeaxanthin > α-carotene > canthaxanthin [6].
The first evidences regarding the effects of polyamines on
carotenoids content in fruits were obtained by Malik and Singh
[22] who found that mango tree treatments by foliar spraying with
Put, Spd, or Spm (0.01, 0.1, and 1 mM) at final fruit set stage
increased total carotenoids in the pulp at harvest time as compared
with fruits from control trees, the main effect being observed with
Put treatments (95%) followed by Spd (33%). More recently, Mehta
et al. [23] reported that ripe fruits from transgenic tomato plants
having the yeast SAMDC gene had higher Spd and Spm concentrations and threefold more lycopene concentration than did the red
fruits from the parental lines. Accordingly, higher levels of polyamines and lycopene were found in transgenic tomatoes overexpressing human SAMDC gene. The increase in lycopene
concentration was attributed to enhanced levels of gene transcripts
involved in lycopene biosynthesis in transgenic tomatoes [24].
Similarly, plants overexpressing mouse ODC gene yielded tomato
fruits with higher polyamine concentration and higher concentration of lycopene as compared with fruits from control plants [25].
These effects of PAs are of special significance since carotenoids,
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Marı́a Serrano and Daniel Valero
including lycopene, are bioactive compounds having antioxidant
capacity and proved beneficial effects in human health [11, 12, 26].
On the contrary, pre- and postharvest Put application to “Angelino” plum led to a linear reduction in the levels of carotenoids,
which were more pronounced with increased concentrations of Put
and storage periods [27]. This effect could be due to the inhibition
of ethylene production and postharvest ripening process as a consequence of Put treatments, since carotenoids increase during ripening and during postharvest storage in plum fruits [6, 16].
3.2 Phenolic
Compounds
Phenolic or polyphenolics are secondary plant metabolites that
exhibit a wide range of physiological roles in plants such as pigmentation, growth, and resistance to pathogens, among many other
functions. The main phenolics in fruits and vegetables are classified
according to their basic skeleton as C6-C1 (phenolic acids), C6-C3
(hydroxycinnamic acids), C6-C2-C6 (stilbenes), and C6-C3-C6 (flavonoids). Phenolics as a group represent the strongest antioxidants
in plant foods, although the antioxidant activity of individual phenolic compounds may vary depending on their chemical structure.
The antioxidant activity of phenolics is attributable to the electron
delocalization over the aromatic ring and their high redox potential, which allows them to act as reducing agents, hydrogen donors,
and singlet oxygen quenchers. Generally, total phenolics increase as
ripening advanced for most fruits, although concentration depends
on several factors including species, cultivar, growth conditions,
and environmental factors [6, 16, 28].
Different effects of polyamine treatment on phenolic content
of fruits have been reported depending on the applied polyamine,
concentration, moment of application, and fruit species. Thus, in
table grape postharvest Spm treatment at 0.5 and 1 mM maintained
total phenol concentration over the controls along 75 days of cold
storage, while Spm at 1.5 mM reduced significantly the berry
phenolic content [29]. On the other hand, postharvest Put treatment at 2 mM of table grapes maintained higher concentration
(1.5-fold with respect to controls) of total phenolics during lowtemperature (0 C) storage [30]. These authors also measured the
individual concentration of catechin (flavonoid) and observed that
it was maintained at higher concentration (twofold) after 60 days of
cold storage +5 days of shelf life, which was correlated with the
higher total antioxidant activity obtained at the end of the experiment. In other two table grape cultivars, polyamines have been also
applied as pre-harvest treatments (40 and 20 days before harvest) at
1 or 2 mM, and results revealed that treated berries showed higher
antioxidant activity and total phenolics at harvest and during cold
storage, although the effectiveness of the treatments was affected
by cultivar, polyamine type, and concentration [31].
In mango, total phenolics and total antioxidant capacity
increased during ripening at ambient temperature and during
Application of Polyamines to Maintain Functional Properties in Stored Fruits
453
cold storage at 11 C although these increases were higher in fruits
treated with Put at 0.5, 1, 1.5, and 2 mM before storage [1]. By
other hand, in kiwifruit total phenolics decreased during storage at
room temperature, although the application of Spd or Spm (0.5, 1
and 1.5 mM), by dipping treatment previously to storage, led to
retention of total phenolic concentration along storage, the main
positive effect being found for Spm at 1.5 mM [33]. Similar results
were observed in pomegranate as a consequence of Put or Spd
postharvest treatments, Spd treatment being more effective than
Put treatment when applied as vacuum infiltration [34]. On the
contrary, Koushesh-saba et al. [35] reported lower phenolic content in Put- and Spd-treated apricots than in controls. Thus, the
effects of polyamines on total phenolic content (TPC) remain
elusive.
3.3
Anthocyanins
Anthocyanins are the water-soluble pigments responsible for the
red, blue, and purple colour of fruits, and have been described as
potent antioxidants. Anthocyanins are located in the vacuole and
classified as flavonoids with glycosilated derivatives of the 3,5,7,30 tetrahydroxyflavylium cation. The free aglycones (anthocyanidins)
are highly reactive with sugars to form the glycosides and all anthocyanins are O-glycosilated. The main aglycones found in fruits are
pelargonidin, cyanidin, peonidin, delphinidin, petunidin, and malvidin while the most relevant sugars are D-glucose, L-rhamnose, Dgalactose, D-xylose, and arabinose [36]. Anthocyanins have shown
higher antioxidant activity than other phenolic compounds, with
cyanidin being the most common anthocyanidin and the 3glucoside the most active anthocyanin with antioxidant activity [6].
Pre-harvest treatment with Put or Spd (at 1 or 2 mM) of
“Olhoghi” and “Rishbaba” table grape cultivars led to berries
with higher content of anthocyanins at harvest, especially for
2 mM Put [31]. These authors also found that after 55 days of
cold storage, anthocyanin concentrations had decreased in control
berries while remained at significant higher levels in all Put- or Spdtreated ones, probably due to the effect of polyamines on delaying
the postharvest ripening process. In table grape “Flame Seedless”
cultivar, it has been reported that postharvest Spm treatment (0.5,
1 and 1.5 mM) induced a progressive increase in total anthocyanins
during prolonged storage, while in control samples there was an
initial increase (during 45 days of storage) but a sharp decrease
occurred during next 30 days (end of the experiment) of storage.
Interestingly, the effect of Spm treatment on increasing berry
anthocyanin concentration was dose-dependent [29].
In addition, in “Mollar de Elche” pomegranate, postharvest
treatments with Put or Spd at 1 mM (either by dipping or infiltration under low pressure) maintained the concentration of aril
anthocyanins during cold storage with respect to controls [34]. In
other pomegranate cultivar (“Mridula”) treatment by immersion
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Marı́a Serrano and Daniel Valero
with 2 mM Put retained also higher anthocyanin during postharvest storage leading to arils with higher antioxidant activity [37].
The mechanism by which Put and Spd induce these effects is still
unknown, although they may be related to their antisenescent
effects related to the suppression of membrane lipid peroxidation
and maintenance of the integrity of membranes [6, 38].
3.4
Vitamins
Vitamins are a group of nutrients necessary for human body due to
their biochemical and physiological functions. Vitamins are classified into lipid-soluble and water soluble, the vitamins A, D, E, and
K being lipophilic, while C and B are hydrophilic. Tocopherols
(vitamin E) are the major lipid-soluble antioxidant vitamins in
fruits, while vitamin C is the major hydrophilic antioxidant vitamin,
although recent evidences indicate that vitamin D could also have a
role as antioxidant [39].
With respect to the relation and/or effect of polyamines in
ascorbic acid content of fruits, it has been found that in transgenic
tomato plants, overexpressing mouse ODC gene, tomato fruits had
higher polyamine concentration than those of the wild type, which
was correlated with an increase in ascorbic acid content as compared with fruits from control plants [25]. Similarly, genetic modification of tomato fruit ripening by overexpressing human-SAMDC
led to higher endogenous levels of polyamines and enhancement of
ascorbic acid content [24]. This increase in ascorbic acid content in
transgenic tomatoes was attributed to their lower ethylene production with respect to the wild type, since ascorbic acid is used as a
cofactor for 1-aminociclopropane-1-carboxilic acid oxidase, the last
enzyme in the ethylene biosynthesis pathway.
By other hand, in two tomato cultivars, postharvest treatments
with Put or Spd (at 1 or 2 mM) did not affect ascorbic acid
concentration, although the combination of both polyamines significantly increased the level of ascorbic acid during 15 or 25 days of
storage at 2 C, especially for the combination of Put
1 mM + Spd2 mM [40].
In pomegranate, treatment with Spd alone or in combination
with calcium chloride showed a net increase in ascorbic acid content
in the arils during 4 months of storage at 2 C [41]. Accordingly,
postharvest treatment of pomegranates with 2 mM Put alone or in
combination with carnauba wax revealed that ascorbic acid declining trend was much pronounced in control as compared to that
found in treated fruit arils, either in pomegranates stored at chilling
temperature (3 C) or at safe temperature (5 C). Among the
applied treatments, the combination of Put and carnauba wax
gave the best results in terms of ascorbic acid retention at 3 and
5 C storage temperatures [37]. Postharvest treatments with Put or
Spd at 1 mM (either by immersion or vacuum-infiltration) in
“Mollar de Elche” pomegranate induced higher content of ascorbic
acid which was detected immediately 1 day after treatments and
Application of Polyamines to Maintain Functional Properties in Stored Fruits
455
lasted along storage, the effect being higher in those fruits treated
under vacuum-infiltration [34].
These effects of PAs increasing or maintaining high ascorbic
acid content during storage are of special interest, since ascorbic
acid is a bioactive compound with antioxidant capacity and proved
beneficial effects in human health [11, 12].
4
Polyamines and Antioxidant Enzymes
In plant cells, the reactive oxygen species (ROS), such as superoxide
radical (O2 #), peroxide radical (O2 2#), hydrogen peroxide
(H2O2), and hydroxyl radical (OH #), are randomly generated as
a consequence of normal metabolism, mainly in reactions catalyzed
by oxidase and lipoxygenase and in ß-oxidation of fatty acids. The
ROS content in plant cell is dependent on their producing systems
and scavenging mechanism, both enzymatic and non-enzymatic
ones [42]. As commented above, non-enzymatic antioxidant compounds are reduced forms of ascorbate and glutathione, tocopherols, phenolics, alkaloids, and carotenoids. In addition, at
physiological concentrations, polyamines are potent scavengers of
hydroxyl radicals while Spd and Spm are also able to quench both
singlet oxygen and hydrogen peroxide [43]. By other hand, enzymatic scavenging mechanisms include mainly superoxide dismutase
(SOD), catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX). SOD detoxifies O2 # free radicals by converting them
to O2 and H2O2, which is further converted to H2O and O2 by
CAT, APX, and POD. CAT catalyzes the decomposition of hydrogen peroxide to water and oxygen, while APX uses ascorbate and
H2O2 as substrates producing water and dehydroascorbate as products, the last one being converted to ascorbate by glutathione
reductase enzyme. In addition, H2O2 can be also reduced to
water by POD, by using organic molecules such as phenols as
electron donor [44].
In this sense, it has been reported that treatment of cherry
tomatoes with arginine, the amino acid precursor of polyamines,
resulted in increased SOD, CAT, and APX activities compared with
the control, which were associated with the reduction of chilling
injury development in treated fruit [45]. Moreover, in tomato
plants under drought stress, an increase in Put and Spd concentrations were found in tomato fruit, as well as in the activities of SOD
and CAT, the latter being responsible for the reduction in the
oxidative damage induced by the stress conditions [46].
In mango, the activity of SOD, POD and CAT increased
during ripening at ambient temperature and during cold storage
at 11 C although these increases were higher after treatments with
Put at 0.5, 1, 1.5, and 2 mM [32]. Similarly, higher activities of
CAT, POD and SOD were found in two apricot cultivars
l
l
l
l
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Marı́a Serrano and Daniel Valero
(“Bagheri” and “Asgarabadi”) during storage at 1 C plus 2 days at
20 C treated with 1 mM Put or Spd than in control fruits, which
were related to a higher resistance to stress and a longer commercial
life [35]. These studies reveal that postharvest polyamine treatment
increases the ability of fruit tissues to eliminate ROS and contributes to alleviate the chilling injury (CI) symptoms observed in
control fruits.
Thus, the effects of exogenous application of polyamines on
increasing the antioxidant enzyme activities would lead to preserve
membrane integrity and to reduce accumulation of ROS and in
turn to alleviate fruit stress, especially chilling injury, as well as to
delay the postharvest ripening process with additional benefits on
maintaining fruit quality properties during postharvest storage.
5
Conclusions
In this chapter we provide the recent information regarding the
effect of polyamines on maintaining functional properties in stored
fruits. With respect to the non-enzymatic antioxidant systems, the
exogenous application of polyamines, as pre- or postharvest treatments, generally resulted in increases on the content of antioxidant
compounds such as phenolics (including anthocyanins), carotenoids, and vitamins, especially ascorbic acid. On the other hand,
polyamines are also effective on increasing the activity of several
antioxidant enzymes, such as SOD, CAT, POD, and APX. Both
systems could contribute to cleaning the ROS generated during the
postharvest ripening process, and in turn to delay the postharvest
ripening and senescence processes and extending the shelf life of
fruits. Nevertheless, the precise physiological and molecular
mechanisms by which polyamines increase both antioxidant systems remain elusive and deserve further research.
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