Postharvest Biology and Technology 115 (2016) 38–47

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Postharvest Biology and Technology

journal homepage: www.elsevier.com/locate/postharvbio

The effect of chilling injury-inducing storage conditions on quality and

consumer acceptance of different Prunus persica cultivars
Jordi Giné-Bordonaba* , Celia M. Cantín, Gemma Echeverría, Dolors Ubach,
Christian Larrigaudière
Institute for Food and Agricultural Research and Technology (IRTA), Parc Científic i Tecnològic Agroalimentari de Lleida, Edifici Fruitcentre, 25003 Lleida, Spain

A R T I C L E I N F O A B S T R A C T

Article history: Few information is available about how chilling injury-inducing storage affects quality and consumer
Received 1 September 2015 acceptance of different peach/nectarine cultivars and its possible relationship with altered physiological
Received in revised form 7 December 2015 or ripening-related events. Accordingly, this study investigated the effect of chilling injury (CI)-inducing
Accepted 8 December 2015
temperatures (4  C during 21 days) on ethylene production, firmness loss, ACC oxidase (ACO) activity,
Available online xxx
antioxidant capacity, chilling injury symptoms such as mealiness or flesh browning, sensory attributes
and consumer acceptance of six melting (‘Ambra’, ‘Nectaross’, ‘Rome Star’, ‘Big Top’, ‘Honey Royale’ and
Keywords:
‘Sweet Dream’) and a stony-hard (SH; ‘Ghiaccio-1’) peach/nectarine cultivars, over two consecutive
Antioxidant capacity
Chilling injury
seasons (2011–2012). Cold storage at 4  C induced greater ethylene production and ACO activity
Ethylene accompanied by greater firmness loss in all cultivars except for the SH phenotype. Antioxidant capacity
Melting-flesh slightly decreased in response to cold storage, but increased during shelf life (20  C) after 1 or 3 days to
Stony-hard reach similar levels than those observed in non-cold stored fruit. The greatest capacity of the fruit to
produce ethylene after cold storage was associated to lower mealiness incidence. For most cultivars,
chilling injury-inducing storage negatively influenced the consumer acceptability. However, no clear
relationships were found between the antioxidant capacity, the pattern of firmness loss and the
development of chilling injury symptoms.
ã 2015 Elsevier B.V. All rights reserved.

1. Introduction production and by maintaining high firmness values during

postharvest storage (Hagi et al., 2001a,b; Begheldo et al., 2008).
Peach and nectarine (Prunus persica L. Batsch) are classified as SH is believed to result from a mutation impairing ethylene
climacteric fruit, in which a sharp increase in ethylene production production. In fact, exogenous application of ethylene to SH fruit
is considered to control the initiation of the ripening process has demonstrated to promote post-harvest softening (Hagi et al.,
(Amorós et al., 1989; Tonutti et al., 1991). In addition, peach fruit 2001a,b; Hayama et al., 2006).
texture is usually classified into melting-flesh (MF), non-melting Regardless of their flesh texture and due to their high
flesh (NMF) or stony-hard (SH). The MF type is characterized by a perishability, peach and nectarine are stored for different time
rapid loss of firmness whereas the NMF type is characterized by a at low temperatures to slow down metabolism, impairing ethylene
more limited softening (Tonutti et al., 1996; Begheldo et al., 2008) production, and extending the commercial life of the fruit.
with mature fruit from both typologies producing ethylene as fruit However, temperatures in the range of 2–8  C may result in the
ripens. The melting and non-melting together with the freestone/ development of chilling injury (CI) in susceptible cultivars
clingstone character, are controlled by the so-called Freestone- (Crisosto et al., 1999b; Cantín et al., 2010). CI may manifest as
Melting flesh locus on stone fruit chromosome 4 (Ogundiwin et al., the lost of ability to soften normally, the appearance of flesh
2009). This gene encodes the cell wall pectin-cleaving enzyme, browning (FB), and development of mealy (M) or woolly texture
known as endopolygalacturonase (endoPG), and also plays a major (Lurie and Crisosto, 2005). Besides, CI seems to generally affect MF
role in the fruit softening of many other fruit crops. In contrast, SH due to an exaggerated expansion of the intercellular spaces in the
genotypes are characterised by the absence of both ethylene fruit mesocarp (Brovelli et al., 1998). However, the capability of the
fruit to produce certain amounts of ethylene during storage, as
observed in NMF genotypes, has been earlier referred as beneficial
to prevent CI (Lurie and Crisosto, 2005). MF cultivars vary in their
* Corresponding author. Fax: +34 973 23 83 01.
E-mail address: [email protected] (J. Giné-Bordonaba).
susceptibility to CI, with some cultivars exhibiting symptoms in all

http://dx.doi.org/10.1016/j.postharvbio.2015.12.006
0925-5214/ ã 2015 Elsevier B.V. All rights reserved.
 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47 39

fruit after only one week of cold storage, even at 0  C, while others maturity of each individual fruit, based on the index of absorbance
withstanding six weeks of cold storage before eventually ripening difference (IAD = A670 A720; DA-Meter, TR Turoni, Forli, Italy), was
and senescing (Cantin et al., 2010; Crisosto et al., 1999b). The assessed and fruit with homogenous medium apparent maturity
development of CI symptoms during storage, mainly M and FB, has (based on a normal distribution) were selected for further analysis
been previously associated with reduced perception of normal and storage. Then, selected fruit (n = 280) were individually
flavour and with development of off-flavours hence affecting weighed, labelled and stored at 20  C immediately after harvest
consumer perception (Crisosto, 2002). Thus said, different or after 21 days of storage at 4  C (considered as CI-inducing
cultivars respond differently to chilling-inducing storage con- conditions in contrast to 0  C which is the recommended storage
ditions and little information is available in terms of its effect on temperature for peaches) and samples were taken after 1, 3 and
consumer acceptance. 5 days, respectively. All quality measurements and consumer
The aim of this study was to investigate how postharvest acceptance were determined on the same 20 fruit per cultivar at
storage at chilling-inducing temperatures affected fruit ripening each evaluation time (n = 160). In parallel, flesh tissue from five
(ethylene production and firmness loss), overall quality, antioxi- individual fruit per replicate, and three replicates per cultivar and
dant capacity, the development of CI symptoms and consumer sampling date (n = 120), was frozen in liquid nitrogen and kept at
acceptance of different melting flesh cultivars as well as a SH 80  C until further biochemical analysis.
phenotype. A further objective was to investigate whether the fruit
antioxidant capacity or the capacity to produce ethylene were 2.2. Fruit quality and chilling injury symptoms evaluation
directly related to CI susceptibility.
Total soluble solids (TSS;%) were measured on peach juice
2. Materials and methods (blend of 5 fruits per replicate and 4 replicates per sampling) using
a digital hand-held refractometer (Atago, Tokyo, Japan) whereas
2.1. Plant materials and storage conditions acid content (TTA) was measured on the same juice samples by
titration using NaOH 0.1N and results expressed as g malic acid g 1
Fruit from seven cultivars (n > 700 per cultivar; Table 1) were sample. Objective colour values (L*, a* and b*) were measured
harvested at optimum commercial maturity, in accordance to using a portable spectrophotometer CM-2600d (Konica Minolta
growers recommendations. Fruit were harvested from local Sensing, Japan) covering the range of wavelengths between
orchards situated in the region of Lleida (Catalonia, North-East 360 and 740 nm. All colour measurements were taken on two
Spain) over two consecutive seasons (2011 and 2012), except for equatorial sides of each fruit (n = 20).
‘Ghiaccio-1’ which was evaluated only in 2012 and the number of The flesh browning and mealiness index (related to CI) were
fruit available was lower. After each harvest date, the apparent individually determined subjectively for each cultivar (by assess-
ing visually 20 individual fruit per cultivar) after 21 days of cold
storage at 4  C plus subsequent 5 days at 20  C to allow CI
Table 1
Firmness (N) (average  SD), DA-value (min–max), ethylene (mL kg 1 h 1; average symptoms to be noticeable. In detail, flesh browning was scored in
 SD) and harvest date in the different cultivars investigated in 2011 and 2012. a 0–4 visual scale as follows: 0 = no browning; 1 = 0–25% surface
Measurements for firmness and DA were taken immediately after harvest while the affected; 2 = 26–50%; 3 = 51–75%; 4 > 76%. Mealiness was also
ethylene production was measured after 2 days of storage at 20  C. scored in a 0–4 visual scale as follows: 0 = no mealy; 1 = slightly
Cultivar Attribute 2011 2012 mealy/elastic fruit; 2 = moderately mealy; 3 = mealy (little amount
Ambra Firmness 52.04  9.01 47.7  6.72
of juice released) and 4 = completely mealy (almost no juice
DA-value 0.56–0.81 0.63–0.86 released).
Ethylene 2.92  0.81 4.73  1.11
Harvest date 28- Jun 02- Jul 2.3. Flesh firmness, ethylene production and ACO activity
Big Top Firmness 51.54  5.2 56.1  4.7
DA-value 0.7–0.98 0.57–0.89 Non-destructive firmness was evaluated in two opposite sides
Ethylene 1.02  0.10 0.5  0.23 of each fruit using an acoustic firmness sensor (AFM, AWETA) as
Harvest date 28-Jun 04-Jul well as a 5% deformation test using a food texture analyser (TA-
XT2, Stable Micro System). Then, fruit firmness of the same fruit
Nectaross Firmness 56.93  10.4 61.3  8.87
DA-value 0.52–0.83 0.62–0.89
was determined destructively using a hand-held penetrometer
Ethylene 1.27  0.73 1.51  0.30 fitted with an 8-mm diameter plunger, after removing the peel of
Harvest date 27- Jul 01-Aug the fruit on two opposed sides. Results were expressed in Newtons
(N).
Honey Royale Firmness 40.51  5.19 53.6  7.14
Ethylene production (mL kg 1 h 1) was measured in an
DA-value 0.64–0.93 0.55–0.87
Ethylene 0.42  0.05 0.76  0.23 acclimatized chamber at 20  C. Three replicates of two fruits each
Harvest date 28- Jul 01-Aug were placed in 1.5 L flasks continuously ventilated with humidified
air at a flow rate of 1.5 L h 1. Then, gas samples (1 mL) were taken
Rome Star Firmness 53.21  7.15 52.4  6.47 daily from the headspace and injected into a gas chromatograph
DA-value 0.51–0.95 0.66–0.97
Ethylene 1.51  0.33 3.07  1.78
fitted with a FID detector (Agilent Technologies 6890, Wilmington,
Harvest date 20- Jul 24- Jul Germany) and an alumina column 80/100 (2 m  3 mm) (Teknok-
roma, Barcelona, Spain) as previously described (Giné Bordonaba
Sweet Dream Firmness 54.09  5.97 43.5  4.76 et al., 2014).
DA-value 0.7–1.2 0.68–0.99
ACO activity was extracted as described by Chiriboga et al.
Ethylene 0.37  0.21 3.1  0.74
Harvest date 25- Jul 26- Jul (2013) and the enzyme activity analysed mixing 500 ml aliquot of
the enzyme extract with 10 mM FeSO4, 3 mM sodium bicarbonate
Ghiaccio-1 Firmness – 37.5  7.90 and 50 mM ACC. The mixture was aired and incubated for 20 min at
DA-value – – 26  C, after which a 1 mL headspace gas sample was injected into a
Ethylene – 1.89  0.42
Harvest date – 20- Jul
gas chromatograph and the results were expressed as nmol
C2H4 g 1 h 1.
40 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47

2.4. Quantification of total antioxidant capacity

Ambra Big Top
70 70
Fruit antioxidant capacity was measured using the FRAP assay S

as described in earlier works (Terry et al., 2007; Giné Bordonaba 60 60

and Terry, 2009) with some modifications. A 50 mL aliquot of
M

Firmness (N)

Firmness (N)
diluted sample extract (1:9; v/v) or Fe2+ (FeSO4
7H20) standards 50 50

(0–5.0 mM) was added to 3.6 mL of freshly prepared FRAP working 40 40

solution (viz. 5 mL of 10 mM TPTZ (2,4,6-tripyridyl-2-triazine) in
40 mM HCl + 5 mL of 10 mM FeCl3 in 50 mL of 300 mM acetate 30 30
buffer). The reaction mixture was incubated at 37  C for 10 min and
20 20
absorbance measured spectrophotometrically at 593 nm using a
PowerWave HT Microplate Spectrophotometer (BioTek Instru- 10 10
ments Inc., Winooski, USA). Antioxidant capacity was expressed as
the concentration of antioxidants having a ferric reducing ability 0 0
(mg Fe3+ g 1 FW). Nectarross Honey Royale
70 70

2.5. Consumer tests 60 60

Firmness (N)

Firmness (N)
For consumer evaluation, fruit samples from all cultivars, except 50 50
Ghiaccio-1 due to the limited number of fruit available, were 40 40
assessed immediately after harvest and after 21 days of cold
storage, and after following 1, 3 and 5 days at 20  C. Prior to 30 30
evaluation, flesh firmness was measured and two longitudinal
20 20
wedges were instrumentally analysed in relation to its SSC and TA
values; the rest of the fruit was divided in pieces and used for 10 10
consumer evaluation. Fruit samples were placed on white plates
and immediately presented to a panel of 50 consumers. The 0 0
consumers were the same for all the evaluations assessed and were Rome Star Sweet Dream
volunteers from the staff working at IRTA (Institut de Recerca i 70 70
Tecnologia Agroalimentàries) and the University of Lleida and 60 60
students from the University of Lleida. All participants were
Firmness (N)

Firmness (N)
regular peach consumers. Each piece was identified by a random 50 50
three-digit code and the order of presentation of the pieces
40 40
presented was randomized for each taster. Mineral water was used
as a palate cleanser between tastings. Each consumer assessed all 30 30
the samples and was asked to indicate his/her degree of liking/
disliking using a 9-point hedonic scale (1 = dislike extremely to 20 20
9 = like extremely). Crispness, firmness and juiciness were also 10 10
evaluated with a 5-point hedonic scale (1 = no perception to
5 = strong perception of each attribute considered). The samples 0 0
0 1 2 3 4 5 6
could be re-tasted as often as desired. Ghiaccio-1
70 Days at 20ºC
2.6. Data analysis
60

Data were subjected to analysis of variance (ANOVA) tests using

Firmness (N)

50
JMP 8.0.1 SAS Institute Inc. Least significant difference values (LSD;
p  0.05) were calculated for mean separation using critical values 40
of t for two-tailed tests. Correlations between experimental
30
variables were made using Spearman’s Rank Correlations and, if
required, presented as Spearman’s Correlation Coefficient (r) and P 20
value based on a two-tailed test. Unless otherwise stated,
significant differences were p  0.05. Unscrambler version 10
9.1.2 software (CAMO, 2004) was used to develop a Partial Least 0
Square Regression model (PLSR). The PLSR was used as a predictive 0 1 2 3 4 5 6
method to relate consumer’s likeness (Y) to a set of explanatory Days at 20ºC
variables (X) which contains physicochemical measures and
sensory attributes. Fig. 1. Firmness loss during storage at 20  C in Prunus persica fruit from different
cultivars over two consecutive harvest years (2011 (*) and 2012 (~)) before (black
symbols) and after (white symbols) 21 days of cold storage (4  C). In cultivar ‘Ambra’
3. Results both the theoretical softening (S) and melting (M) phases are depicted.

3.1. Fruit softening, ethylene production and ACO activity after harvest

The loss of firmness observed herein followed a typical biphasic ‘Big Top’, ‘Honey Royale’ and ‘Sweet Dream’. Based on these
pattern for most cultivars (Fig. 1) with an initial slow rate (referred patterns of firmness loss, the above-mentioned cultivars may be
as softening) followed by a rapid decrease of firmness in the case of considered as fast or slow-melting, respectively. As expected,
‘Ambra’, ‘Nectarross’ and ‘Rome Star’, or a moderate decrease for almost no softening was observed in the SH cultivar ‘Ghiaccio-1’.
 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47 41

No obvious relationships between the decrease of firmness and firmness loss (‘Ambra’, ‘Nectarross’, ‘Rome Star’ and ‘Sweet
the onset of ethylene production were observed for most of the Dream’). In contrast, ‘Big Top’ and ‘Honey Royale’ fruit needed 9
cultivars investigated. Generally, fruit held at 20  C immediately and 6 days, respectively, to produce comparable amounts of
after harvest produced little or no ethylene during storage (Fig. 2 ethylene (data not shown). As expected, no ethylene production
and Table 1). However, after 4 days of storage at 20  C, a small but was detected in fruit from the stony-hard phenotype ‘Ghiaccio-1’.
significant rise in ethylene production (>2.5 mL kg 1 h 1) was only No obvious differential patterns were either observed for slow- or
observed for those cultivars experiencing the greatest rate of fast-melting cultivars when studying ACO activity levels (Fig. 3).
Indeed, ACO activity at harvest was minimal in ‘Big Top’ (0.2 nmol
C2H4 g 1 h 1) but among the greatest in ‘Honey Royale’ (1.16 nmol
C2H4 g 1 h 1) or the SH ‘Ghiaccio-1’ (1.25 nmol C2H4 g 1 h 1).
For most cultivars, the rate and pattern of firmness loss was
similar between years except for ‘Big Top’ and ‘Sweet Dream’
where significant year-to-year variations were noticed. Fruit from
‘Big Top’ fruit harvested on 2011 reached eating quality (8.8–17.6 N;
(Crisosto et al., 1999a)) after 6 days of storage (Fig. 1) whereas no
firmness changes until day 7 were observed in fruit from the same
orchard and cultivar harvested on the following year. A similar
variability between years was also observed in ‘Sweet Dream’ but
in this case fruit from 2011 remained firmer during storage at 20  C
if compared to fruit harvested on the following year which reached
eating quality after 5d (Fig. 1). Accompanying the year-to-year
variation in terms of firmness, ethylene production (absolute
values but not the ethylene production pattern), was also different
between years for each cultivar (Fig. 2).

3.2. Fruit softening, ethylene production and ACO activity after cold
storage

If compared to storage at 20  C immediately following harvest,

differences in the softening behaviour between the different
cultivars were less apparent after 21 days of storage at 4  C, when
softening occurred in a faster pace (Fig. 1). A loss of firmness during
cold storage was also generally observed if comparing firmness
values at harvest and after cold storage for most cultivars but
specially in ‘Ambra’, ‘Honey Royale’ and ‘Rome Star’.
A substantial increase in ethylene production during shelf life
was observed in response to chilling injury-inducing storage
conditions for most cultivars, except for the stony hard ‘Ghiaccio-1’
(Fig. 2). Ethylene production was ca. 20-fold greater in fruit from
cultivars ‘Big Top’ and ‘Ambra’ following three weeks of cold
storage and some days at 20  C if compared to values at harvest. In
addition, after three weeks of storage at 4  C ethylene production
was also greatest in ‘Big Top’ and ‘Ambra’ with maximum ethylene
values occurring at day 4 (220 mL kg 1 h 1) and day 5 (210 mL
kg 1 h 1), respectively, and being 5-fold greater than the values
observed for the rest of cultivars.
Accompanying the increase in ethylene production, 3 weeks of
cold storage at 4  C prior to storage at 20  C also induced greater
ACO levels (Fig. 2) for some but not all the cultivars. In the case of
‘Big Top’, more than 10-fold greater levels of ACO were observed
after cold storage, whereas a 2-fold increase was observed for
‘Ambra’ and ‘Honey Royale’ cultivars.

3.3. Chilling injury incidence

Different susceptibility to chilling injury (CI) after storage at

4  C was observed among the different cultivars (Table 2). ‘Ambra’,
‘Big Top’, ‘Nectarross’ and ‘Honey Royale’ showed none or very
slight browning, whereas ‘Sweet Dream’ and ‘Ghiaccio 1’ showed
moderate and intense browning, respectively. On the other hand,
no mealiness incidence was observed in ‘Ambra’ and ‘Big Top’
cultivars, whereas high incidence was observed in ‘Nectarross’,
‘Honey Royale’, ‘Rome Star’ and ‘Sweet Dream’ fruit. Due to the lack
Fig. 2. Ethylene production (mL kg 1 h 1; average  SD) in fruit from the seven
peach/nectarine cultivars at 2 consecutive harvest years (2011 (*) and 2012 (~))
of softening in the ‘Ghiaccio 1’ fruit, mealiness incidence could not
during storage at 20  C before (black symbols) and after (white symbols) 21 days of be evaluated.
cold storage (4  C).
42 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47

3.0

2.5

ACO (nmol C2H4 g h )

-1 -1 2.0

1.5

1.0

0.5

0.0

am
p

1
ar
e
ss
a
br

al
To

o
St
ro

oy

re

ci
Am

ar
ig

ac
tD
R

om
B

hi
ec

ey

ee

G
R
N

on

Sw
H

Fig. 3. ACC oxidase (nmol C2H4 g 1 h 1; average  SD) in fruit from the seven peach/nectarine cultivars before (&) and after ( ) 21 days of storage at chilling inducing
temperatures (4  C). Single error bar depicts LSD value (p < 0.05) for the interaction cultivar*storage scenario.

juiciness after cold storage was noticed by the consumers. As

Table 2
Chilling injury incidence, measured on the basis of flesh browning and mealiness
observed by the sensory measurement of firmness, a certain
(average  SD), after 21 days of cold storage at 4  C plus 5 days at 20  C. Different degree of firmness loss was perceived by the consumers after
letters within a column mean statistical significant differences (p  0.05). storage at 20  C. However, no significant changes were described
Cultivar Browning Mealiness
after cold storage compared to harvest. In contrast, consumers
perceived a more obvious firmness loss in ‘Honey Royale’ after cold
Ambra 0a 1.7  1.0ab
Big Top 0a 0.7  0.7a
storage than during ripening at 20  C.
Nectarross 0a 3.5  1.3b For ‘Ambra’ and ‘Nectarross’ the crispness loss was mainly
Honey Royale 0.75  0.4b 3.2  1.5b affected by ripening period at 20  C regardless of the cold storage.
Rome Star 1.85  1.1bc 4.0  0.0bc In contrast, in ‘Big Top’, ‘Rome Star’, ‘Honey Royale’ and ‘Sweet
Sweet Dream 2.95  0.9c 3.2  1.4b
Dream’ cold storage appeared to be necessary to induce crispness
Ghiaccio 1 3.20  1.3cd –
loss.
Regarding consumer acceptability, only fruit from ‘Nectarross’
3.4. Antioxidant capacity and ‘Ambra’, before cold storage (Table 3), were below the limit of
acceptability. In general, consumer acceptability increased during
Albeit only measured with one in vitro assay, noticeable (and shelf life at 20  C for all the cultivars, with the exception of ‘Big Top’.
sometimes significant) differences in the fruit antioxidant capacity On the contrary, cold storage resulted in lower consumer
were observed among cultivars (Fig. 4). The highest levels were acceptance for most cultivars but again except for ‘Big Top’.
observed in ‘Ambra’, ‘Big Top’ and ‘Sweet Dream’ cultivars, whereas
the lowest were observed in ‘Nectarross’ and ‘Honey Royale’. No 3.6. The role of some sensory attributes and physicochemical
significant changes were observed for the fruit antioxidant parameters in consumer likeness
capacity during shelf life for any cultivar investigated. The cold
storage period in general reduced the antioxidant capacity of the A Partial Least Squares regression (PLSR) model was built up in
fruit, especially in the fruit from ‘Ambra’ and ‘Big Top’, where an attempt to correlate consumer likeness (Y variable) with a set of
significantly lower levels were observed after 21 days of cold potentially explanatory variables (X variables) which included:
storage if compared to the levels observed after harvest (Fig. 4). physicochemical parameters and sensory attributes. These varia-
bles accounted for 55% of the variability in likeness (Fig. 5). This
3.5. Sensory attributes and consumer acceptability value was almost twice that of variance in likeness explained by
juiciness, which was the explanatory variable that correlated best
Cold storage significantly influenced the juiciness attribute with likeness (r2 = 0.28). The validation step indicated that two PLS
perceived by the consumers in some cultivars (Table 3), especially factors were relevant in the model. Cultivar and cold storage was
the cultivars with more mealiness incidence as ‘Nectarross’ and the main factor for sample differentiation along PC1 which
‘Honey Royale’. In those cultivars, juiciness attribute score accounted alone for 44% of total variability. Fruit of ‘Big Top’,
decreased from 3.4 and 3.9, respectively after 5 days at 20  C to ‘Honey Royale’ and ‘Sweet Dream’ were located more on the right
2.1 after 21 + 3days, when CI symptoms were already perceptible. side of the PC1 (Fig. 5A). The corresponding loadings plot (Fig. 5B)
However, although mealiness incidence was also observed in shows that these samples obtained higher likeness scores, were
‘Sweet Dream’ fruit after 21 + 5 days, no significant decrease of perceived by the consumer as being juicier, crisper and firmer, and
 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47 43

1.0 1.0
Ambra Big Top

Antioxidant capacity (mg Fe /g)

Antioxidant capacity (mg Fe2+/g)
0.8 0.8

2+
0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0

Nectarross Honey Royale

Antioxidant capacity (mg Fe2+/g)

Antioxidant capacity (mg Fe2+/g)

0.8 0.8

0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0

Rome Star Sweet Dream

Antioxidant capacity (mg Fe2+/g)

Antioxidant capacity (mg Fe /g)

0.8 0.8

2+
0.6 0.6

0.4 0.4

0.2 0.2

0.0 0.0
0 1 3 5
Ghiaccio-1
Days at 20ºC
Antioxidant capacity (mg Fe2+/g)

0.8

0.6

0.4

0.2

0.0
0 1 3 5

Days at 20ºC

Fig. 4. Antioxidant capacity (mg Fe3+ g 1 FW; average  SD) of the seven peach/nectarine cultivars when stored for 0, 1, 3 or 5 days at 20  C either before (&) or after ( ) 21
days of cold storage at 4  C. Single error bar for each cultivar depicts LSD (p < 0.05) for the interaction storage scenario*days at 20  C.
44 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47

Table 3
Likeness and sensory attributes of the fruit from different cultivars at harvest (0), after 1, 3, 5 days of storage at 20  C (1, 3 and 5), after 21 days of cold storage at 4  C (21 + 0) and
after 21 days of cold storage plus 1, 3 and 5 days at 20  C (21 + 1, 21 + 3 and 21 + 5). Likeness was scored using a 9-point hedonic scale and sensory attributes with a 5-point
hedonic scale.

0 1 3 5 21 + 0 21 + 1 21 + 3 21 + 5
Likeness
Ambra 3.9 cB 4.6 cdB 5.1 cB 5.3 bB 4.6 cB 3.9 cdB 6.7 abA 5.1 abB
Big Top 6.3 aBC 6.2 abBC 5.8 bcBC 5.3 bC 6.9 aAB 7.0 aAB 7.8 aA 6.3 aBC
Rome Star 4.2 cCD 5.0 bcBC 6.2 abcAB 7.2 aA 4.9 bcBC 3.5 dCDE 3.3 dDE 2.1 cE
Honey Royale 5.9 abB 6.6 aAB 7.7 aA 7.8 aA 6.7 aAB 5.6 bB 3.8 cdC
Nectarross 3.8 cBC 3.6 dBC 5.5 bcA 4.7 bABC 4.8 bcAB 4.4 cdABC 5.4 bcA 3.4 cC
Sweet Dream 4.8 bcCD 5.0 bcBCD 6.7 abA 6.9aA 5.9 abABC 5.3 bcBCD 6.1 bAB 4.1 bcD

Juiciness
Ambra 2.8 aDE 3.1 abCD 3.7 aBC 4.3 aA 2.8 aD 2.0 cE 3.7 bBC 4.0 abAB
Big Top 3.1 aBC 2.6 bC 2.5 bC 2.5 cC 3.0 aBC 3.2 aB 4.5 aA 4.5 aA
Rome Star 2.6 aB 2.9 abAB 3.4 aAB 3.8 abA 2.9 aAB 2.6 abcB 3.0 bcAB 2.4 cB
Honey Royale 3.0 aBC 3.5 aAB 3.1 abAB 3.9 abA 3.4 aAB 3.0 abBC 2.1 cC
Nectarross 2.5 aC 2.8 abBC 3.8 aA 3.4 bAB 2.7 aBC 2.5 bcC 2.1 cC 2.5 cC
Sweet Dream 2.7 aA 3.0 abA 3.2 aA 2.0 cB 3.3 aA 3.0 abA 3.4 bA 3.3 bcA

Firmness
Ambra 4.5 aA 4.0 bA 1.7 cD 1.8 cCD 3.2 bcB 2.5 bBC 2.0 bcCD 1.5 abD
Big Top 4.4 aAB 4.6 aA 4.4 aAB 4.4 aAB 4.0 aBC 3.8 aC 2.8 aD 1.8 aE
Rome Star 4.5 aA 3.5 cBC 3.3 bCD 2.7 bD 4.0 aAB 1.8 bE 1.6 cE 1.2 bE
Honey Royale 4.2 aA 4.1 abA 4.0 aA 3.0 bB 2.8 cB 2.4 bBC 1.9 bcC
Nectarross 4.1 aA 4.2 abA 2.8 bCD 2.6 bD 3.9 aAB 3.4 aBC 2.6 abD 1.3 bE
Sweet Dream 4.3 aA 4.2 abA 4.0 aA 4.4 aAB 3.8 abAB 4.0 aA 3.3 aB 1.5 abC

Crispness
Ambra 4.8 aA 4.1 bA 1.6 dD 1.7 cD 3.1 bcB 2.5 cdBC 1.9 bCD 1.3 abD
Big Top 4.5 abA 4.7 abA 4.5 aA 4.3 aA 3.6 abB 3.0 bcBC 2.8 aC 1.6 aD
Rome Star 4.1 bA 3.4 cAB 3.0 bcBC 2.4 bCD 4.0 aA 1.8 dDE 1.5 bE 1.0 bE
Honey Royale 4.3 bA 4.2 abA 3.7 bA 2.9 bB 2.8 cB 2.6 cB 1.6 bC
Nectarross 4.2 bA 4.2 abA 2.2 cdD 2.2 bcD 4.0 aAB 3.4 bBC 2.8 aCD 1.2 bE
Sweet Dream 4.5 abA 4.8 aA 4.5 aA 4.6 aA 4.3 aA 4.2 aA 3.3 aB 1.5 abC

Means for a given sensory parameter within the same column followed by different small letters and within the same row followed by different capital letters are significantly
different at p  0.05 (Tukey’s HSD test).

presented higher TSS and firmness instrumental values than the climacteric (Tonutti et al., 1996) yet no clear relationships were
rest of cultivars. However, fruit stored for 21 d at 4  C and ripen for observed in the results presented herein for most of the cultivars.
3 or 5 d at 20  C, and therefore susceptible to CI symptoms, were In agreement with the differential ethylene production pattern
positioned in the left part of PC1 (second and third quadrant), far among cultivars, Ghiani et al. (2011) reported that fast-melting
away from the likeness, firmness and crispness attributes, except flesh fruit from cv. ‘Bolero’ was observed to produce ethylene at
for ‘Big Top’ and ‘Sweet Dream’ (only for 21 + 3 days). harvest, whereas 4 days, at least, were necessary for the slow-
Fig. 6 shows the regression coefficients for likeness versus the melting flesh ‘Big Top’ fruit to initiate ethylene production. These
rest of the variables. It may be observed that consumer likeness authors also found that the slow-melting flesh trait, as in ‘Big Top’,
was positively related to juiciness and TSS concentration, and appeared to be linked to a delayed 1-aminocyclopropane-1-
negatively related to IAD thereby indicating that consumer likeness carboxylic acid synthase (ACS) or reduced ACC oxidase (ACO)
was associated with normal fruit ripening. expression and the resulting delayed ethylene evolution. In the
In conclusion, consumer likeness was mainly influenced by present study, ethylene production was also delayed in fruit from
cultivar and storage. Cold-storage negatively influenced consumer slow-melting cultivars (‘Honey Royale’ and ‘Big Top’) but no
perception once the CI symptoms were noticeable after ripening. associations were found with ACO levels. Indeed, ACO levels at
Shelf-life also affected consumer likeness leading to significant harvest were minimal in ‘Big Top’ (0.2 nmol C2H4 g 1 h 1) but
changes in TTA, TSS (data not shown) and firmness values and in a among the greatest in ‘Honey Royale’ (1.16 nmol C2H4 g 1 h 1) or
more intense perception of some sensory attributes. the stony-hard ‘Ghiaccio-1’ (1.25 nmol C2H4 g 1 h 1). Based on our
results and in agreement with Ghiani et al. (2011), it may be that
4. Discussion ACS, but not ACO, is the key enzyme limiting the production of
ethylene in slow-melting or stony-hard cultivars. Collectively, our
Little is still known about the exact biochemical or physiological results confirm that the softening experienced by stone fruit after
changes responsible for the abnormal ripening in response to harvest is not exclusively dependent on ethylene production.
storage at CI-inducing temperatures or the influence that different The less noticeable differences in the softening behaviour of the
texture fruit types may have in the susceptibility to CI. Accordingly, different cultivars after storage at 4  C, suggest that cold storage at
we investigated how chilling injury-inducing storage at 4  C this chilling-inducing temperature may directly cause important
affected the fruit physiology and biochemistry and the develop- structural changes within the fruit. Changes in peach firmness
ment of CI in fruit from seven different softening-type peach and following cold storage have been related to modifications in the
nectarine cultivars. content of pectins bound covalently to the cell wall as well as
The rapid (i.e. ‘Ambra’ and ‘Nectarross’) or moderate (i.e. ‘Big altered cell wall-modifying enzymes activities (Ortiz et al., 2011;
Top’ and ‘Honey Royale’) decrease of fruit firmness after harvest is Zhang et al., 2010). Consistently, Endo- and Exo-polygalacturonase
thought to be in correspondence to the onset of the ethylene (PG) activities have been reported to be less abundant in woolly or
 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47 45

Fig. 5. Scores (A) and loadings (B) plot of PC1 versus PC2 corresponding to a PLSR model for consumer likeness versus physicochemical parameters and sensory attributes.
Cultivars codes: Ambra (AM); Big Top (BT); Nectarross (NR); Honey Royale (HR); Rome Star (RS) and Sweet Dream (SD). Storage codes: At harvest (0), at harvest plus 1, 3, 5 days
of storage at 20  C (1, 3 and 5), after 21 days of cold storage at 4  C (21 + 0) and after 21 days of cold storage plus 1, 3 and 5 days at 20  C (21 + 1, 21 + 3 and 21 + 5).

mealy fruit when compared to juicy fruit (Zhou et al., 2000; documented (Lelievre et al., 1997; Villalobos-Acuna et al., 2011;
Obenland et al., 2003; Brummell et al., 2004). In turn, Endo- and Chiriboga et al., 2013). Nonetheless, information regarding the
Exo-PG activities are known to be positively modulated by cold-induced ethylene metabolism in peach is scarce (Dong et al.,
ethylene (Hayama et al., 2006). In agreement, our results 2001). From our results, it is evident that the cold-induced
demonstrate that the amount or rate of ethylene production after ethylene burst was not always accompanied by an increased in ACO
cold storage was negatively correlated to the development of activity and hence other regulatory factors may account for the
mealiness symptoms. Fruit showing the greatest ethylene produc- greater levels of ethylene detected after cold storage.
tion after cold storage had the lowest incidence of this disorder. In Recently, Pávez et al. (2003) showed that during chilling injury-
other species (i.e. pear) the cold-induced ethylene production inducing cold storage, several genes linked to the oxidative stress
accompanied by higher expression of both ACS and ACO is well response increased in abundance therefore suggesting changes in
46 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47

Fig. 6. Regression coefficients corresponding to a PLSR model for consumer likeness versus physicochemical parameters and sensory attributes.

fruit redox or antioxidant status which in turn accounted for the product in question has a soft melting texture, as in the case of
abnormal ripening of mealy fruit. However, no direct relationship peach (Harker et al., 2002). A marked reduction in juiciness is often
between the incidence of mealiness and the fruit antioxidant associated with texture disorders in stone fruit (Harker et al., 1997),
capacity, as determined by the FRAP assay, were observed in this as the mealiness or wooliness induced by CI. Our results completed
study. Our results are in accordance with the inconsistent results this observation and also show the influence of the development of
found in the literature when studying the effect of cold storage in CI symptoms on the perception of juiciness by the final consumer.
the antioxidant metabolism of several peach and nectarine Sweetness showed also a large relation to consumer likeness as
cultivars (Wang et al., 2006; Meng et al., 2009; Tsantili et al., it has already been reported in other peach and nectarine cultivars
2010). Moreover, our data reveals no clear relationship between (Infante et al., 2008; Ortiz et al., 2009; Di Miceli et al., 2010).
fruit antioxidant capacity and the development of any CI Moreover, it has been described that high contents of sugars
symptoms. It is however likely that specific antioxidants (either (sucrose and glucose) alleviate CI symptoms in peach fruit, because
enzymatic or not), rather than the fruit antioxidant capacity, are carbohydrates may serve as osmoregulators and cryoprotectants
key in the prevention of abnormal ripening and the development contributing to membrane stability. Besides, carbohydrates may
of chilling injury disorders. It is also apparent that chilling inducing act as scavengers of reactive oxygen species, and sugar metabolism
conditions have an influence not only in one aspect of the fruit might provide reducing power to the ascorbate–glutathione cycle
metabolism but in several simultaneously, hence making it protecting cells against chilling stress (Van den Ende and Valluru,
complicated to find out the exact relationships between CI 2009; Abidi et al., 2015). Our PLS results agree with these data since
symptoms and fruit specific compounds/parameters. the most susceptible cultivars localize in opposed quadrants
In addition to changes in fruit redox status, Pávez et al. (2003) respect to the TSS parameter.
suggested that woolly fruit had lower expression levels of genes To summarize, this work demonstrates that chilling injury-
involved in aroma production, and therefore, lower levels of the inducing storage have a differential effect depending on the
volatile compounds that would normally confer the characteristic cultivar on the fruit ethylene production capacity, the rate of
aromatic properties of a ripe fruit. Indeed, the effect of cold storage softening and the fruit antioxidant capacity. In addition, there are
on the volatile production of peaches and nectarines is well changes in certain fruit attributes (mainly juiciness, firmness and
documented (Robertson et al., 1990; Aubert et al., 2003; Raffo et al., TSS) during cold storage which negatively affect its consumer
2008; Infante et al., 2008; Ortiz et al., 2009, 2011; Yang et al., 2009; acceptance. The capacity of the fruit to produce ethylene is not
Zhang et al., 2010, 2011; Cano-Salazar et al., 2012). The lack of some clearly linked to the rate of softening within the melting-flesh type
characteristic aroma compounds as reported by Pávez et al. (2013), fruit (slow- or fast-melting) but plays a determining role on the
together with low juiciness and sweetness perception (Cano- development of certain chilling injury symptoms (i.e. mealiness).
Salazar et al., 2013) may account for the lower consumer Further studies are needed to deep in the physiological and
acceptance observed for most cultivars after chilling injury- biochemical changes induced by cold storage, with special
inducing storage. Thus said, our PLS results indicate that the fruit emphasis on fruit ethylene and antioxidant metabolism, and their
juiciness and the TSS content as well as both the sensory and possible influence on CI susceptibility.
instrumental firmness were the main variables affecting consumer
likeness. For the majority of fruit ‘juiciness’ is a principal texture Acknowledgement
attribute. There are few, if any, other foods that can match most
fruit for the intensity of this attribute. Consumers expect fruit to This work has been partly supported by the EU seventh
provide a sensation of juiciness irrespective of whether the Framework Programme through the FruitBreedomics project no.
 J. Giné-Bordonaba et al. / Postharvest Biology and Technology 115 (2016) 38–47 47

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