Trends in Food Science & Technology 21 (2010) 599e606
Review
Advances on
polyphenols and their
metabolism in
sub-tropical and
tropical fruits
Dominique Rinaldoa,*,
Didier Mbéguié-A-Mbéguiéb
and Bernard Fils-Lycaona
a
INRA, UMR 1270 Qualité des fruits et légumes
tropicaux, Domaine de Duclos, F-97170 Petit-Bourg,
Guadeloupe, France
(Tel.: D33 590255926; fax: D33 590255415;
e-mail: Dominique.Rinaldo@antilles.inra.fr)
b coupled reactions, leading to brown pigments.
CIRAD, Station de Neufchâteau, F-97130 Capesterre,
Guadeloupe, France
Today consumers are more and more concerned with food
components providing health beneficial effects, such as poly-
phenols. Polyphenols also influence the organoleptic quality
of plant-derived food, including fruits. Most studies on poly-
phenols content and composition have been carried out on
fruits grown in temperate countries. Less is known on polyphe-
nols in tropical fruits. This paper summarises knowledge on
polyphenol composition and metabolism in tropical and
sub-tropical fruits in relation to ripening and storage condi-
tions. As tropical fruits are highly susceptible to browning,
a particular interest is drawn on the respective influence of
biochemical parameters responsible for browning.
Introduction: interest for polyphenols in food
Vitamins, carotenoids and polyphenols are known to
contribute to health beneficial effects related to the con-
sumption of plant-derived food in relation to their antioxi-
dant properties (Sun, Chu, Xianzhong, & Liu, 2002). In
* Corresponding author.
0924-2244/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tifs.2010.09.002
particular, all fruits and vegetable contain a great variety
of polyphenols, which are important secondary metabolites
of plants. The antioxidant activities of plant-food have been
related to their total phenolic content but also to their com-
position in phenolic compounds (Tomas-Barberan & Espin,
2001). These compounds are also responsible for a wide
range of organoleptic characteristics, such as color, bitter-
ness and astringency. There is a lack of knowledge on phe-
nolic compound composition of food. Most studies have
dealt with rather simple compounds that can be assayed
by High Performance Liquid Chromatography (HPLC),
such as phenolic acids and flavonoids. Less is known about
tannins which are polymers whose composition in constitu-
tive units is seldom determined (Cheynier, 2005). More-
over, the polyphenolic composition of food can be
changed by storage and conservation conditions and by pro-
cessing. These changes are mainly due to numerous enzy-
matic and non-enzymatic reactions to which polyphenols
are highly susceptible. One of these reactions is, at first
step, the enzymatic oxidation of o-diphenols to o-quinones
by polyphenol oxidase (PPO), followed by non-enzymatic
Among plant-derived foods, fruits are of high interest as
they are richer in polyphenols than vegetables and contrib-
ute to polyphenol dietary intake at the same level as bever-
ages (Scalbert & Williamson, 2000). However, most studies
on polyphenol composition of fruits were concerned with
those grown in temperate countries, such as grape, apple
or pear (Gu et al., 2004). Less interest has been drawn on
fruits from tropical areas, whereas they are more and
more often commercialized all over the world. This paper
aims to sum up the knowledge about phenolic composition
and metabolism in sub-tropical and tropical fruits in rela-
tion with cultivars, ripening and storage conditions.
Polyphenolic composition of tropical fruits
Recent interest has been drawn on the determination of
the polyphenolic composition of tropical and sub-tropical
fruits. Table 1 presents the polyphenols unambiguously
identified in the flesh of these fruits. The identification
was assayed by HPLC with diode array detection and
mass spectrometry (MS) and then nuclear magnetic reso-
nance (NMR) spectrometry was added if required. In these
conditions, only in a few species, such as mango, cashew
apple and andean blackberry, the polyphenolic profile has
been almost completed. In others, such as banana, acerola
600 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
Table 1. Unambiguously identified polyphenols in the pulp of some fresh tropical fruits. The polyphenols were identified using high-
performance liquid chromatography and mass spectrometry, NMR was added if required
Tropical fruit Phenolics
Andean blackberry Phenolic acids: gallic and ellagic acids and
their conjugates, p-coumaric,
ferulic and caffeic esters
Hydrolysable tannins: ellagitannins
Flavonols: quercetin glycosides,
kaempferol glycosides
Anthocyanins: cyanidin-3-glucoside,
cyanidin-3-rutinoside
Flavanols: epicatechin
Acerola Anthocyanins: cyanidin 3-rhamnoside,
pelargonidin 3-rhamnoside
Cashew apple Phenolic acids: gallic and p-coumaric
acids and conjugates
Flavonols: myricetin and quercetin glycosides
Condensed tannins: Highly polymerised
prodelphinidins (epigallocatechin and
epigallocatechin 3-O-gallate) and procyanidins
Banana Catecholamine: dopamine
Condensed tannins: controversial
data on their composition
Mango Hydrolysable tannins: 8 gallo-tanins
(tetra to heptamers)
Phenolic acids: gallic acid, ellagic acid
C-glucosyl xanthone: mangiferin
Flavonols: quercetin 3-O-glucoside,
quercetin 3-O-galactoside
Mountain papaya Phenolic acids: 10 ferulic acid glycosides
or sinapic acid glycosides
Flavonols: 9 quercetin glycosides
including rutin and manghaslin
Star fruit Hydrolysable tannins: gallotannins
Flavanols and tannins: epicatechin,
dimers to pentamers of catechin or/and epicatechin
and star fruit, a part of the polyphenol families has been as-
sayed. Moreover, in mountain papaya (Carica pubescens),
star fruit and sapodilla the polyphenols which have been
unambiguously identified have not been quantified yet
(Table 1). Table 2 presents the tentatively identified poly-
phenols in the flesh of fruits. The polyphenols showed in
this table were obtained using HPLC and compared to stan-
dards. To our knowledge, in pineapple, guava and papaya
(Carica papaya), none of the polyphenols has been unam-
biguously identified. It is noticeable that when only HPLC
was used, only flavonols aglycons, which corresponded to
available standards, were found in banana, cashew apple,
guava and papaya. However, it is well known that flavonols
are often linked to glycosides. It can thus be suspected that
in these fruits some compounds are still unknown and fur-
ther formal identification by MS and NMR methods is re-
quired. Studies on the phenolic compounds of tropical
fruits are at the beginning and more studies are therefore
needed to characterize the polyphenolic composition of
these fruits. It is noteworthy that two main polyphenol fam-
ilies can be synthesised by two different pathways, one
leading to catecholamines from tyrosine and the other
one to phenylpropanoids from phenylalanine. The pulp of
Content (mg/100 g FW) Authors
7.6e22.7 Mertz, Cheynier, Günata,
& Brat, 2007
178e520
9.8e14.2
126e177
0.9e1.1
31.3e63.4 Sousa de Brito et al., 2007
0.4 Michodjehoun-Mestres, Souquet,
Fulcrand, Bouchut, et al., 2009
0.3 Michodjehoun-Mestres, Souquet,
2.0 Fulcrand, Meudec, et al., 2009
0.7e10 Kanazawa & Sakakibara, 2000;
4 Tanaka, Kondou, & Kouno, 2000;
Gu et al., 2004
2 Berardini, Carle, & Schieber, 2004
0.4 Berardini et al., 2005
0.15
Not quantified Simirgiotis, Caligari,
& Schmeda-Hirschmann, 2009
Not quantified Shui & Leong, 2004
ripe banana (Musa Cavendishii) is rich in catecholamines,
mainly dopamine and L-dopa (Gonzalez-Montelongo,
Lobo, & Gonzalez, 2010), which respectively amounted
on average 7 and 1.6 mg per 100 g of fresh weight (FW)
(Kanazawa & Sakakibara, 2000).
The polyphenolic composition of tropical fruits highly
varies with the species, the cultivar and the tissue. Glycosyl-
flavanones are the most abundant flavonoids in Citrus fruits
and are classified according to their glycoside form, either
neohesperidose, linked to a bitter taste, or rutinose (Tripoli,
La Guardia, Giammanco, Di Majo, & Giammanco, 2007).
A principal component analysis dealing with 45 Citrus spe-
cies has showed that the content in these two glycoside forms
is specific for each Citrus species (Nogata et al., 2006). More-
over, a peculiar molecular structure of flavonoids has been
observed in bergamot, Marsh grapefruit and sour orange,
whereas anthocyanins were found in blood oranges
(Rapisarda, Fabroni, Peterek, Russo, & Mock, 2009). Con-
cerning cultivars, in acerola, cyanidin and pelargonidin gly-
cosides were 20-fold higher in some cultivars than in others
(Hanamura, Uchida, & Aoki, 2008). In mango flesh, over
five cultivars, only the Haden one provided both mangiferin
and quercetin glycosides whereas in the other four only
 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
Table 2. Tentatively identified polyphenols in the pulp of some fresh tropical fruits. The polyphenols were only assayed by high-performance
liquid chromatography using standards
Tropical fruit Phenolics
Acerola Phenolic acids: ferulic, p-coumaric,
chlorogenic acids
Flavonol: quercetin-3-rhamnoside
Condensed tannins: polymers of
catechin and epicatechin
Banana Flavonols: quercetin, myricetin, kaempferol
Catecholamine: dopa, norepinephrine
Cashew apple Flavonol: kaempferol
Citrus fruits Phenolic acids: chlorogenic, caffeic, p-coumaric,
ferulic and sinapic acids
Various species Flavanones: hesperidin, naringin, neohesperidin
Flavonols: kaempferol, quercetin,
quercetin-3-rutinoside
Blood oranges Flavones: diosmin, luteolin, sinensetin
Also contain anthocyanins: cyanidin and
delphinidin glycosides
Guava Flavonols: quercetin
Papaya Flavonols: myricetin, quercetin,
kaempferol, morin
Pineapple Flavonol: quercetin, morin
mangiferin was detected (Berardini et al., 2005). As far as tis-
sues are concerned, the flesh is generally the poorest in poly-
phenols, as shown in banana and mango (Berardini et al.,
2005; Kanazawa & Sakakibara, 2000). As an example, the
mangiferin content of mango peel varied from 1 to 280-
fold that of the flesh, according to cultivars (Berardini
et al., 2005).
Metabolism of phenolic compounds in tropical fruits
As far as synthesis is considered, the enzymes catalysing
the production of catecholamines from tyrosine have been
scarcely described in plants. More is known about PAL
(phenylalanine ammonia-lyase, EC 4.3.1.5), the key en-
zyme for the synthesis of phenylpropanoids. It catalyses
the deamination of phenylalanine, thus producing trans-
cinnamate. As far as catabolism is concerned, PPO (cate-
chol oxidase, EC1.14.18.1.) can convert monophenols to
o-diphenols and it can further oxidize o-diphenols into qui-
nones. The latter polymerizes nonenzymatically into brown
pigments. Peroxidase (POD, EC 1.11.1.7) can also oxidize
phenolic substrates into quinones and be involved in brown-
ing reactions (Marquès, Fleuriet, & Macheix, 2006).
Synthesis
In most temperate plants species, PAL is encoded by
a small multigene family of 2e6 members (Cramer et al.,
1989), which are differentially expressed in plant tissues.
Studies have led to its isolation and characterization at both
molecular and biochemical levels, including the immunoloc-
alization of PAL protein at plasmic membrane (Davin &
Lewis, 1991). There are fewer data on PAL enzyme charac-
teristics in tropical fruits (Diallinas & Kanellis, 1994).
601
Content (mg/100 g FW) Authors
1e31 Hanamura et al., 2008
Mezadri, Villano, Fernandez-Pachon,
1.5e11 Garcia-Parrilla, & Troncoso, 2008
3e14
0.4e2 Kanazawa & Sakakibara, 2000;
Kevers et al., 2007
2.2e3.1 Lako et al., 2007
<0.3 Hoffmann-Ribani, Huber,
& Rodriguez-Amaya, 2009
0.01e0.03 Y.-C. Wang, Chuang, & Ku, 2007
0.05e0.65
0.02e0.19
0.01e0.08
Rapisarda et al., 2009
1.1 Hoffmann-Ribani et al., 2009
9 Lako et al., 2007
3 Lako et al., 2007
Oxidation of phenolics
Browning is due to the oxidation of phenolics. Data sug-
gest that browning depends on various factors such as total
phenolic content, its compounds composition and PPO ac-
tivity (Jayaraman & Ramanuja, 1987; Maneenuam, Ketsa,
& van Doorn, 2007; Trakulnaleumsai, Ketsa, & van
Doorn, 2006). As PPO is localized on the thylakoid mem-
brane of chloroplasts and polyphenols are in the vacuole,
a cellular loss of compartmentation is also needed to
make PPO oxidize its substrates (Tomas-Barberan &
Espin, 2001). Due to discrepancy between cultivars and
species, further studies are needed to know more about
the link between browning and all these factors.
The biochemical characterization of PPO enzyme has
been performed in various tropical fruits, including banana,
avocado and mango pulp (Gomez-Lopez, 2002; J. Wang
et al., 2007; Yang, Fujita, Ashrafuzzaman, Nakamura, &
Hayashi, 2000) and litchi pericarp (Liu et al., 2010). The mo-
lecular weight of PPO determined by gel filtration in banana
pulp was about 41 kDa. Optimum pH was found to vary from
6.5 in banana to 7.5 in avocado. Km (Michaelis-constant)
values indicated that substrates specificity widely changed
from one species to another. The best specificity was obtained
with dopamine in banana (Yang et al., 2000). In the particular
case of litchi pericarp, browning in post-harvest is said to be
due to the oxidation of anthocyanin (red pigments). However,
it has been recently shown that PPO cannot directly oxidize
a major anthocyanin of litchi pericarp, cyanidin 3-rutinoside
(Liu, Cao, Xie, Sun, & Wu, 2007) and the direct substrate for
PPO in this fruit was ( )-epicatechin (Liu et al., 2010). A
model for the degradation of anthocyanin has been
established with a coupled oxidation mechanism involving
the ( )-epicatechin o-quinone generated by PPO. The
602 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
post-harvest browning of litchi pericarp may also be related
to a lesser extent, to some flavonols, such as quercetin 3-ru-
tinoside, whose ortho-diphenolic structure may lead to a sus-
ceptibility to oxidation by PPO (Sarni-Manchado, Le Roux,
Le Guernevé, Lozano, & Cheynier, 2000). More knowledge
is thus required both about PPO substrates in vivo and
their interactions with other polyphenols which may be in-
volved in the non-enzymatic oxidation mechanisms.
The large studies devoted to the biochemical character-
ization of PPO enzyme in tropical fruits were in contrast
with the lesser interest drawn by molecular studies of
PPO. Besides tropical fruits, genes encoding PPO have
been isolated and characterized from a wide range of plants
and generally include multigene families. Conversely, PPO
protein is encoded by one gene in cherimoya genome
(Prieto et al., 2007), and by a small multigene family of
at least two and four members in banana and pineapple,
respectively (Gooding, Bird, & Robinson, 2001; Zhou,
Dahler, Underhill, & Wills, 2003). For the last two species,
analysis of the corresponding genomic sequence of PPO
genes indicated the presence of a single intron in contrast
with genomic sequences of PPO genes isolated from others
species. As observed in other species, PPO members of
genes are differentially regulated in tropical fruits accord-
ing to the tissue and to biotic or abiotic stresses.
Information about POD characteristics and its substrates
in tropical fruits are scarce. However, it was demonstrated
that POD cannot directly oxidize anthocyanin in litchi peri-
carp. A coupled oxidation mechanism involving POD
might lead to pericarp browning, as reported for PPO
(Zhang, Pang, Xuewu, Ji, & Jiang, 2005).
Influence of post-harvest factors on the total phenolic
content and the metabolism of polyphenols
The major limit to international trading of tropical fruits
is their susceptibility to transport and storage conditions.
Most tropical fruits ripen and deteriorate quickly at ambient
temperature. Cold storage is used to slow down these
processes and increase the fruits lifetime after harvest.
However, most tropical fruits are susceptible to low temper-
atures, which induce chilling injury, a physiological disor-
der that often leads to browning (Lurie & Crisosto,
2005). Fruits browning in post-harvest can also be due to
wounding and induces a rejection of the fruit by consumers.
Some studies on tropical fruits have therefore dealt with
changes in polyphenols and their metabolism due to post-
harvest ripening and storage conditions.
Ripening
In banana, when fruits were harvested at the mature-
green stage and ripened at room temperature, a marked
increase in total phenolic content of the pulp was found be-
tween the initial and the fully ripe stages (Giami & Alu,
1994). In senescent Cavendish bananas, a similar rise in to-
tal phenolic content was observed with the development of
peel spotting (Choehom, Ketsa, & van Doorn, 2004). In
contrast, a 52% decrease in total phenolic content was
found during the ripening of sapote mamey at 9th day
post-harvest (Alia-Tejacal et al., 2007). These controversial
data suggested that changes in total phenolic content during
ripening might be highly dependent on the fruit species.
Little information is available on shifts in polyphenolic
composition during ripening at room temperature.
When loquat fruit were placed at 20  C to ripen, its PAL
protein activity transiently increased, reaching its maxi-
mum after harvest and then going back to its initial level
2 days later (Cai, Xu, Li, Ferguson, & Chen, 2006). This
finding, which reflected an enhanced synthesis of phenyl-
propanoids soon after harvest, was concomitant with
a higher lignin content and firmness of loquat fruit. Similar
data were previously reported in melon fruits, showing that
PAL transcript levels were low in young fruits, exhibited
a peak during ripening at the climacteric maximum and de-
clined again in overripe fruits (Diallinas & Kanellis, 1994).
According to these authors, the changes in PAL protein ac-
tivity with the ripening stage were related to the expression
of genes for ethylene biosynthesis. Later in ripening, PAL
enzyme activity was stable in senescent Cavendish banana
ripened at room temperature, which was not consistent with
the concomitant increase in total phenolic content previ-
ously reported (Choehom et al., 2004). Further studies are
needed to follow PAL protein activity all over ripening,
from the mature-green to the overripe stages.
During ripening at room temperature, Gooding et al.
(2001) found a high but stable PPO activity in Cavendish
banana whereas a marked increase was reported in the
peel of over-ripped spotting bananas (Choehom et al.,
2004; Trakulnaleumsai et al., 2006). This is in disagree-
ment with the concomitant raise in total phenolic content
previously reported. Browning of banana fruit during ripen-
ing might be due to the release of a pre-existing PPO syn-
thetised very early in development (Gooding et al., 2001).
This was consistent with the finding of two PPO forms in
loquat fruit, a latent pre-enzyme bound to plastids which
generated a mature soluble active PPO (Sellés-Marchart,
Casado-Vela, & Bru-Martinez, 2006), in good agreement
with previous data in apricots (Chevalier et al., 1999). In lo-
quat fruits, the activity of the latent PPO was optimum at
pH 4 whereas that of the mature form was optimum at
pH 6.5, suggesting that the latent form catalyses rapidly
the oxidation of phenolics in acidic conditions such as tis-
sue disruption. At the molecular level, in banana, although
the activity of the protein remains high during ripening,
PPO genes were down regulated at transcriptional level
(Gooding et al., 2001). In contrast, in pineapple, PPO
gene expression was slightly induced during ripening
(Stewart, Sawyer, Bucheli, & Robinson, 2001).
An increase in POD activity was observed in the
pulp of loquat fruit (Cai et al., 2006) and sapote mamey
(Alia-Tejacal et al., 2007) placed at 20  C or room temper-
ature to ripen, respectively. In sapote mamey, a parallel rise
in PPO activity was reported, supporting the involvement of
 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
both of these enzymes in flesh browning which naturally
occurred during ripening.
Cold storage
Cold storage generally resulted in a marked decrease in to-
tal phenolic content in most fruit studied. This decrease was
observed, after 5e6 days storage at 4e6  C, in the peel of ba-
nana (Nguyen, Ketsa, & van Doorn, 2003) and mango (Kondo,
Kittikorn, & Kanlayanarat, 2005) and in the pericarp of litchi
(Zhang & Quantick, 1997). In litchi, this decrease was linked
to a decline in total flavonoid content (Zhang & Quantick,
1997). In oranges, storage at 6  C for 65 days significantly re-
duced total phenolic content in a blond genotype of the “Valen-
cia Late” variety, whereas it was increased in blood varieties,
mainly due to a 2e9-fold higher content in anthocyanins
(Rapisarda, Lo Bianco, Pannuzzo, & Timpanaro, 2008). These
controversial effects suggest that chilling injury led both to
modifications of phenolic content and composition, which
may depend on the species or variety. Further investigations
on the influence of storage conditions on phenolic composition
of tropical fruits are therefore still needed.
There is a general agreement that PAL protein activity is
enhanced after 7e14 days storage at chilling temperatures,
in the range of 2e13  C, as observed in banana, pineapple
and Annona Cherimola fruit (Maldonado, Molina-Garcia,
Sanchez-Ballesta, Escribano, & Merodio, 2002; Nguyen
et al., 2003; Zhou et al., 2003). In mandarin fruit, an increase
in PAL mRNA was also reported after storage at 2  C
(Sanchez-Ballesta, Zacarias, Granell, & Lafuente, 2000), in
good agreement with recent findings in the pulp of banana
kept at 8  C for twelve days (Chen et al., 2008). These data
suggested that chilling injury involved the stimulation of phe-
nylpropanoid synthesis reflected by the higher PAL protein
activity, as reported in fruits grown in temperate countries
(Tomas-Barberan & Espin, 2001). In citrus, increases in
both PAL protein activity and PAL mRNA (FPAL1 and
FPAL2 mRNA) levels due to chilling temperature, were
shown to be very quick and occurred prior the appearance
of chilling symptoms (Sanchez-Ballesta et al., 2000).
PAL induction can be considered as a defence mecha-
nism against chilling, as it resulted in lower cold-induced
peel damage in mandarin fruit (Lafuente, Zacarias,
Martinez-Téllez, Sanchez-Ballesta, & Dupille, 2001). This
is in good agreement with the high constitutive levels of
PAL transcripts and protein activity found at harvest in a ge-
netically chill-resistant mandarin cultivar (Sanchez-Ballesta
et al., 2000). When the fruits were then stored at a temper-
ature of 2  C, there was no further rise in PAL enzyme ac-
tivity in genetically chill-resistant mandarin cultivars in
contrast to the PAL protein enhancement observed in
chill-susceptible varieties (Sanchez-Ballesta et al., 2000).
Moreover, the older the fruit, the more marked was the abil-
ity of chilling-sensible “Fortune” mandarins to induce PAL
protein activity and transcripts in response to cold stress
(Lafuente, Zacarias, Martinez-Téllez, Sanchez-Ballesta, &
Granell, 2003).
603
During cold storage, the lower total phenolic content re-
ported was consistent with a rise in PPO activity recorded
within the 10e30 days following the exposition to low tem-
perature in fruits such as banana, pineapple and carambola
(Nguyen et al., 2003; Pérez-Tello, Silva-Espinoza, Vargas-
Arispuro, Briceno-Torres, & Martinez-Tellez, 2001; Zhou
et al., 2003). This rise may reflect an increased oxidation
of free phenolics and was due to de novo synthesised en-
zyme. Moreover, this increased oxidation is also linked to
a loss of compartmentation between the enzyme and its
substrates, as it is known that chilling injury induces dete-
rioration in membranes functions thus leading to browning
(Saltveit, 2002). The higher PPO activity during cold stor-
age was correlated to chill-induced peel browning in ba-
nana and to black-heart symptoms in pineapple (Nguyen
et al., 2003; Stewart et al., 2001). It is noticeable that
most authors found higher activities of both PAL and
PPO enzymes in response to cold storage, supporting evi-
dence for a general enhancement in phenolic compounds
metabolism in response to chilling temperatures.
No clear conclusion can be drawn on the involvement of
POD in peel browning at chilling temperatures, as species
showed contrasting responses. Cold storage induced a de-
crease in POD activity of mango kept at 5  C (Ding,
Tian, Zheng, Zhou, & Xu, 2007) whereas it resulted in
a raise in carambola placed at 2  C (Pérez-Tello et al.,
2001). In pineapple, contradictory data on POD activity
were reported (Weerahewa & Adikaram, 2005; Zhou
et al., 2003) and one additional POD isozyme was also
found in tissues undergoing internal browning due to cold
storage, as compared to healthy tissues.
Wounding
Mechanical wounding occurring during transport and
storage leads to browning of the peel or the flesh of fruits
and induces a decreased commercial value. Wounding
caused a seven-fold increase in PAL protein activity and
an accumulation in PAL transcripts in mandarin fruit stored
at 20  C for 27 h (Sanchez-Ballesta et al., 2000). This is in
keeping with previous findings in melon, indicating a no-
ticeable rise in PAL protein content in response to wound-
ing in unripe fruit, while the response was less marked in
ripe fruits (Diallinas & Kanellis, 1994).
PAL protein increase can be considered as a non-specific
defence mechanism used to cope with various environmen-
tal factors, including wounding. All the data previously re-
ported indicate that, as in temperate fruits, expression of
PAL genes in tropical fruits appear to be differentially
regulated at both transcriptional and translational level ac-
cording to biotic and abiotic cues. However, these tran-
scriptional and translational steps might not be the only
ones involved in the regulation of PAL gene expression. In-
deed, a post-translational regulation of PAL activity,
throughout protein phosphorylation mediated by “calcium
dependent protein kinase” has been reported in plants
(Allwood, Davies, Gerrish, & Bolwell, 2002).
604 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
In tropical fruit, wounding differentially affected the PPO
gene expression according to the species. In pineapple flesh,
wounding has been related both to a four-fold increase in
PPO activity and to mRNA PPO induction (Stewart et al.,
2001) whereas no modification of PPO activity was found in
banana (Gooding et al., 2001). In flesh and rind tissues of
wounded cherimoya, the lack of correlation between PPO
mRNA accumulation and the unmodified enzyme activity sug-
gests a post-transcriptional, translational and/or a post-transla-
tional process as key steps of regulation of PPO gene
expression (Prieto et al., 2007). In contrast, all studies per-
formed in pineapple fruit indicated that changes in PPO activity
in this species is regulated at transcriptional level and imply the
de novo protein synthesis of PPO (Stewart et al., 2001).
Conclusion
Sub-tropical and tropical fruits are all the more sensitive to
browning as they risk chilling injury damages and wounding
during transport to foreign countries. As shown by reported
results, further studies are needed to determine whether
browning reaction in post-harvest is linked to the total pheno-
lic content, its compounds composition, activities of oxidative
enzymes or the loss of cell compartmentation. In most sub-
tropical and tropical fruits, the polyphenolic compounds re-
quire further formal identification and/or quantification. At
chilling temperature, the decrease in total phenolic content
is concomitant with an increased PPO activity, which could
result in a higher oxidation of polyphenols. The oxidation
leads both to a modification in phenolic compounds and to
a browning reaction. However, changes in phenolic composi-
tion with ripening and storage conditions have been scarcely
analysed. It is of interest to study these changes, as it will re-
sult in better knowledge about antioxidant properties of fruits,
reflecting their nutritional quality, at the very moment they
are used by consumers. Such studies will also lead to estab-
lish which compounds are responsible for browning reaction.
In particular, better knowledge should be drawn on the iden-
tification of PPO substrates in vivo. The influence of POD in
fruit browning should also be established. Some data indi-
cated that the effects of cold storage on producing fruit
browning and modifying PAL and/or PPO enzymes activities,
could be partly alleviated in banana and avocado (Chen et al.,
2008; Hershkovitz, Saguy, & Pesis, 2005; Nguyen, Ketsa, &
van Doorn, 2004). Further investigations are thus needed to
determine the influence of storage conditions (storage tem-
perature, temperature and chemical pre-treatments, mainly
1-methylcyclopropene, an ethylene action inhibitor, and mod-
ified atmosphere packaging) on browning, polyphenolic com-
position and polyphenol metabolism in tropical fruits.
References
Alia-Tejacal, I., Villanueva-Arce, R., Pelayo-Zaldivar, C., Colinas-
Leon, M. T., Lopez-Martinez, V., & Bautista-Banos, S. (2007).
Postharvest physiology and technology of sapote mamey fruit
(Pouteria Sapota (Jacq.) H.E. Moore and Stearn). Postharvest Biol-
ogy and Technology, 45, 285e297.
Allwood, E. G., Davies, D. R., Gerrish, C., & Bolwell, G. P. (2002).
Regulation of CDPKs, including identification of PAL kinase, in
biotically stressed cells of French bean. Plant Molecular Biology,
49, 533e544.
Berardini, N., Carle, R., & Schieber, A. (2004). Characterization of
gallotannins and benzophenone derivatives from mango (Mangi-
fera indica L. cv. “Tommy Atkins”) peels, pulp and kernels by high-
performance liquid/chromatography/electrospray ionization mass
spectrometry. Rapid Communications in Mass Spectrometry, 18,
2208e2214.
Berardini, N., Fezer, R., Conrad, J., Beifuss, U., Carle, R., &
Schieber, A. (2005). Screening of Mango (Mangifera indica) culti-
vars for their contents of flavonol O- and xanthone C-glycosides,
anthocyanins, and pectin. Journal of Agricultural and Food
Chemistry, 53, 1563e1570.
Cai, C., Xu, C. J., Li, X., Ferguson, I., & Chen, K. S. (2006). Accumu-
lation of lignin in relation to changes in activities of lignification
enzymes in loquat fruit flesh after harvest. Postharvest Biology and
Technology, 40, 163e169.
Chen, J.-Y., He, L.-H., Jiang, Y.-M., Wang, Y., Joyce, D. C., Ji, Z.-L.,
et al. (2008). Role of phenylalanine ammonia-lyase in heat
pretreatment-induced chilling tolerance in banana fruit. Physio-
logia Plantarum, 132, 318e328.
Chevalier, T., de Rigal, D., Mbéguié-A-Mbéguié, D., Gauillard, F.,
Richard-Forget, F., & Fils-Lycaon, B. R. (1999). Molecular cloning
and characterization of apricot fruit polyphenol oxidase. Plant
Physiology, 119, 1261e1269.
Cheynier, V. (2005). Polyphenols in foods are more complex than often
thought. American Journal of Clinical Nutrition, 81(suppl.),
223Se229S.
Choehom, R., Ketsa, S., & van Doorn, W. G. (2004). Senescent spot-
ting of banana peel is inhibited by modified atmosphere packaging.
Postharvest Biology and Technology, 31, 167e175.
Cramer, C. L., Edwards, K., Dron, M., Liang, X., Dildine, S. L.,
Bolwell, G. P., et al. (1989). Phenylalanine ammonia-lyase gene
organisation and structure. Plant Molecular Biology, 12, 367e383.
Davin, L. B., & Lewis, N. G. (1991). Recent advances in phytochem-
istry. New York: Plenum Press.
Diallinas, G., & Kanellis, A. K. (1994). A phenylalanine ammonia-
lyase gene from melon fruit: cDNA cloning, sequence and
expression in response to development and wounding. Plant
Molecular Biology, 26, 473e479.
Ding, Z. S., Tian, S. P., Zheng, X. L., Zhou, Z. W., & Xu, Y. (2007).
Responses of reactive oxygen metabolism and quality in mango
fruit to exogenous oxalic acid or salicylic acid under chilling
temperature stress. Physiologia Plantarum, 130, 112e121.
Giami, S. Y., & Alu, D. A. (1994). Changes in composition and certain
functional properties of ripening plantain (Musa spp., AAB group)
pulp. Food Chemistry, 50, 137e140.
Gomez-Lopez, V. M. (2002). Some biochemical properties of poly-
phenol oxidase from two varieties of avocado. Food Chemistry, 77,
163e169.
Gonzalez-Montelongo, R., Lobo, M. G., & Gonzalez, M. (2010).
Antioxidant activity in banana peel extracts: testing extraction
conditions and related bioactive compounds. Chemistry, 119,
1030e1039.
Gooding, P. S., Bird, C., & Robinson, S. P. (2001). Molecular cloning
and characterisation of banana fruit polyphenoloxidase. Planta,
213, 748e757.
Gu, L., Kelm, M. A., Hammerstone, J. F., Beecher, G., Holden, J.,
Haytowitz, D., et al. (2004). Concentrations of proanthocyanidins
in common foods and estimations of normal consumption. Journal
of Nutrition, 134, 613e617.
Hanamura, T., Uchida, E., & Aoki, H. (2008). Changes of the com-
position in acerola (Malpighia emarginata DC.) fruit in relation to
cultivar, growing region and maturity. Journal of the Science of
Food and Agriculture, 88, 1813e1820.
 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
Hershkovitz, V., Saguy, S. I., & Pesis, E. (2005). Postharvest application
of 1-MCP to improve the quality of various avocado cultivars.
Postharvest Biology and Technology, 37, 252e264.
Hoffmann-Ribani, R., Huber, L. S., & Rodriguez-Amaya, D. B. (2009).
Flavonols in fresh and processed Brazilian fruits. Journal of Food
Composition and Analysis, 22, 263e268.
Jayaraman, K. S., & Ramanuja, M. N. (1987). Changes in polypheno-
loxidase and other endogenous factors during ripening in some
banana varieties. Journal of Food Science and Technology, 24,
67e71.
Kanazawa, K., & Sakakibara, H. (2000). High content of dopamine,
a strong antioxidant, in Cavendish Banana. Journal of Agricultural
and Food Chemistry, 48, 844e848.
Kevers, C., Falkowski, M., Tabart, J., Defraigne, J. O., Dommes, J., &
Pincemail, J. (2007). Evolution of antioxidant capacity during
storage of selected fruits and vegetables. Journal of Agricultural and
Food Chemistry, 55, 8596e8603.
Kondo, S., Kittikorn, M., & Kanlayanarat, S. (2005). Preharvest anti-
oxidant activities of tropical fruit and the effect of low temperature
storage on antioxidants and jasmonates. Postharvest Biology and
Technology, 36, 309e318.
Lafuente, M. T., Zacarias, L., Martinez-Téllez, M. A., Sanchez-
Ballesta, M. T., & Dupille, E. (2001). Phenylalanine ammonia-lyase
as related to ethylene in the development of chilling symptoms
during cold storage of citrus fruits. Journal of Agricultural and Food
Chemistry, 49, 6020e6025.
Lafuente, M. T., Zacarias, L., Martinez-Téllez, M. A., Sanchez-
Ballesta, M. T., & Granell, A. (2003). Phenylalanine ammonia-lyase
and ethylene in relation to chilling injury as affected by fruit age in
citrus. Postharvest Biology and Technology, 29, 308e317.
Lako, J., Trenerry, V. C., Wahlqvist, M., Wattanapenpaibon, N.,
Sotheeswaran, S., & Premier, R. (2007). Phytochemical flavonols,
carotenoids and the antioxidant properties of a wide selection of
Fijian fruit, vegetables and other readily available foods. Food
Chemistry, 101, 1727e1741.
Liu, L., Cao, S., Xie, B., Sun, Z., & Wu, J. (2007). Degradation of
cyanidin 3-rutinoside in the presence of ( )-epicatechin and litchi
pericarp polyphenol oxidase. Journal of Agricultural and Food
Chemistry, 55, 9074e9078.
Liu, L., Cao, S., Xu, Y., Zhang, M., Xiao, G., Deng, Q., et al. (2010).
Oxidation of ( )-epicatechin is a precursor of litchi pericarp
enzymatic browning. Food Chemistry, 118, 508e511.
Lurie, S., & Crisosto, C. H. (2005). Chilling injury in peach and nec-
tarine. Postharvest Biology and Technology, 37, 195e208.
Maldonado, R., Molina-Garcia, A. D., Sanchez-Ballesta, M. T.,
Escribano, M. I., & Merodio, C. (2002). High CO2 atmosphere
modulating the phenolic response associated with cell adhesion
and hardening of Annona cherimola fruit stored at chilling tem-
perature. Journal of Agricultural and Food Chemistry, 50,
7564e7569.
Maneenuam, T., Ketsa, S., & van Doorn, W. G. (2007). High oxygen
levels promote peel spotting in banana fruit. Postharvest Biology
and Technology, 43, 128e132.
Marquès, L., Fleuriet, A., & Macheix, J. J. (2006). In: P. Sarni-Man-
chado, & V. Cheynier (Eds.), Les polyphénols en agroalimentaire
(pp. 135e172). Londres/Paris/New York: Editions Tec. et Doc.,
Lavoisier.
Mertz, C., Cheynier, V., Günata, Z., & Brat, P. (2007). Analysis of phenolic
compounds in two blackberry species (Rubus glaucus and Rubus ad-
enotrichus) by high performance liquid chromatography with diode
array detection and electrospray ion trap mass spectrometry. Journal of
Agricultural and Food Chemistry, 55, 8616e8624.
Mezadri, T., Villano, D., Fernandez-Pachon, M. S., Garcia-
Parrilla, M. C., & Troncoso, A. M. (2008). Antioxidant compounds
and antioxidant activity in acerola (Malpighia emarginata DC.)
fruits and derivatives. Journal of Food Composition and Analysis,
21, 282e290.
605
Michodjehoun-Mestres, L., Souquet, J.-M., Fulcrand, H., Bouchut, C.,
Reynes, M., & Brillouet, J.-M. (2009). Monomeric phenols of
cashew apple (Anacardium occidentale L.). Food Chemistry, 112,
851e857.
Michodjehoun-Mestres, L., Souquet, J.-M., Fulcrand, H., Meudec, E.,
Reynes, M., & Brillouet, J.-M. (2009). Characterization of highly
polymerised prodelphinidins from skin and flesh of four cashew
apple (Anacardium occidentale L.) genotypes. Food Chemistry,
114, 989e995.
Nguyen, T. B. T., Ketsa, S., & van Doorn, W. G. (2003). Relationship
between browning and the activities of polyphenol oxidase and
phenylalanine ammonia lyase in banana peel during low temper-
ature storage. Postharvest Biology and Technology, 30, 187e193.
Nguyen, T. B. T., Ketsa, S., & van Doorn, W. G. (2004). Effect of
modified atmosphere packaging on chilling-induced peel brown-
ing in banana. Postharvest Biology and Technology, 31, 313e317.
Nogata, Y., Sakamoto, K., Shiratsuchi, H., Ishii, T., Yano, M., &
Ohta, H. (2006). Flavonoid composition of fruit tissues of Citrus
species. Biosciences, Biotechnology and Biochemistry, 70,
178e192.
Pérez-Tello, G. O., Silva-Espinoza, B. A., Vargas-Arispuro, I., Briceno-
Torres, B. O., & Martinez-Tellez, M. A. (2001). Effect of tempera-
ture on enzymatic and physiological factors related to chilling
injury in carambola fruit (Averrhoa carambola L.). Biochemical
and Biophysical Research Communications, 287, 846e851.
Prieto, H., Utz, D., Castro, A., Aguirre, C., Gonzalez-Agüero, M.,
Valdés, H., et al. (2007). Browning in Annona cherimola fruit: role
of polyphenol oxidase and characterization of a coding sequence
of the enzyme. Journal of Agricultural and Food Chemistry, 55,
9208e9218.
Rapisarda, P., Fabroni, S., Peterek, S., Russo, G., & Mock, H. P. (2009).
Juice of new citrus hybrids (Citrus clementina Hort. Ex Tan. 
C.sinensis L. Osbeck) as a source of natural antioxidants. Food
Chemistry, 117, 212e218.
Rapisarda, P., Lo Bianco, M., Pannuzzo, P., & Timpanaro, N. (2008).
Effect of cold storage on vitamin C, phenolics and antioxidant ac-
tivity of five orange genotypes [Citrus Sinensis (L.) Osbeck]. Post-
harvest Biology and Technology, 49, 348e354.
Saltveit, M. E. (2002). The rate of ion leakage from chilling-sensitive
tissue does not immediately increase upon exposure to chilling
temperatures. Postharvest Biology and Technology, 26, 295e304.
Sanchez-Ballesta, M. T., Zacarias, L., Granell, A., & Lafuente, M. T.
(2000). Accumulation of PAL transcript and PAL activity as affected
by heat-conditioning and low-temperature storage and its relation
to chilling sensitivity in mandarin fruits. Journal of Agricultural and
Food Chemistry, 48, 2726e2731.
Sarni-Manchado, P., Le Roux, E., Le Guernevé, C., Lozano, Y., &
Cheynier, V. (2000). Phenolic composition of litchi fruit pericarp.
Journal of Agricultural and Food Chemistry, 48, 5995e6002.
Scalbert, A., & Williamson, G. (2000). Dietary intake and bioavail-
ability of polyphenols. Journal of Nutrition, 130, 2073Se2085S.
Sellés-Marchart, S., Casado-Vela, J., & Bru-Martinez, R. (2006). Isolation
of a latent polyphenol oxidase from loquat fruit (Eriobotrya japonica
Lindl.): kinetic characterization and comparison with the active form.
Archives of Biochemistry and Biophysics, 446, 175e185.
Shui, G., & Leong, L. P. (2004). Analysis of polyphenolic antioxidants
in star fruit using liquid chromatography and mass spectrometry.
Journal of Chromatography A, 1022, 67e75.
Simirgiotis, M. J., Caligari, P. D. S., & Schmeda-Hirschmann, G.
(2009). Identification of phenolic compounds from the fruits of the
mountain papaya Vasconcellea pubescens A. DC. grown in Chile
by liquid chromatographyeUV detection-mass spectrometry. Food
Chemistry, 115, 775e784.
Sousa de Brito, E., Pessanha de Araujo, M. C., Alves, R. E., Carkeet, C.,
Clevidence, B. A., & Novotny, J. (2007). Anthocyanins present in
selected tropical fruits: acerola, jambolao, jussara, and guajiru.
Journal of Agricultural and Food Chemistry, 55, 9389e9394.
606 D. Rinaldo et al. / Trends in Food Science & Technology 21 (2010) 599e606
Stewart, R. J., Sawyer, B. J. B., Bucheli, C. S., & Robinson, S. P. (2001).
Polyphenol oxidase is induced by chilling and wounding in pine-
apple. Australian Journal of Plant Physiology, 28, 181e191.
Sun, J., Chu, Y.-F., Xianzhong, W., & Liu, R. H. (2002). Antioxidant and
antiproliferative activities of common fruits. Journal of Agricultural
and Food Chemistry, 50, 7449e7454.
Tanaka, T., Kondou, K., & Kouno, I. (2000). Oxidation and epimeri-
zation of epigallocatechin in banana fruits. Phytochemistry, 53,
311e316.
Tomas-Barberan, F. A., & Espin, J. C. (2001). Phenolic compounds and
related enzymes as determinants of quality in fruits and vegetables.
Journal of the Science of Food and Agriculture, 81, 853e876.
Trakulnaleumsai, C., Ketsa, S., & van Doorn, W. G. (2006). Tempera-
ture effects on peel spotting in ‘Sucrier’ banana fruit. Postharvest
Biology and Technology, 39, 285e290.
Tripoli, E., La Guardia, M., Giammanco, S., Di Majo, D., &
Giammanco, M. (2007). Citrus flavonoids: molecular structure,
biological activity and nutritional properties: a review. Food
Chemistry, 104, 466e479.
Wang, Y.-C., Chuang, Y.-C., & Ku, Y.-H. (2007). Quantitation of bio-
active compounds in citrus fruits cultivated in Taiwan. Food
Chemistry, 102, 1163e1171.
Wang, J., Jiang, W., Wang, B., Liu, S., Gong, Z., & Luo, Y. (2007).
Partial properties of polyphenol oxidase in mango (Mangifera
Indica L. CV. “Tainong”) pulp. Journal of Food Biochemistry, 31,
45e55.
Weerahewa, D., & Adikaram, N. K. B. (2005). Some biochemical
factors underlying the differential susceptibility of two pineapple
cultivars to internal browning disorder. Ceyland Journal of Science
(Biological Science), 34, 7e20.
Yang, C.-P., Fujita, S., Ashrafuzzaman, M. D., Nakamura, N., &
Hayashi, N. (2000). Purification and characterization of polyphe-
nol oxidase from banana (Musa sapientum L.) pulp. Journal of
Agricultural and Food Chemistry, 48, 2732e2735.
Zhang, Z., Pang, X., Xuewu, D., Ji, Z., & Jiang, Y. (2005). Role of
peroxidase in anthocyanin degradation in litchi fruit pericarp. Food
Chemistry, 90, 47e52.
Zhang, D., & Quantick, P. C. (1997). Effects of chitosan coating on
enzymatic browning and decay during postharvest storage of litchi
(Litchi chinensis Sonn.) fruit. Postharvest Biology and Technology,
2, 195e202.
Zhou, Y., Dahler, J. M., Underhill, S. J. R., & Wills, R. B. H. (2003).
Enzymes associated with blackheart development in pineapple
fruit. Food Chemistry, 80, 565e572.