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Scientia Horticulturae 309 (2023) 111668
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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti
Effect of coating with co-product-based bionanocomposites on the quality

of strawberries under refrigerated storage
Rafael Carvalho do Lago a, Elídio Zaidine Maurício Zitha b, Ana Lázara Matos de Oliveira b,
Danilo José Machado de Abreu c, Elisângela Elena Nunes Carvalho b, Roberta Hilsdorf Piccoli b,
Gustavo Henrique Denzin Tonoli a, Eduardo Valério de Barros Vilas Boas b, *
a
Forests Sciences Department, Federal University of Lavras, Cx P. 3037, Lavras, MG CEP 37200-000, Brazil
b
Food Science Department, Federal University of Lavras, Cx P. 3037, Lavras, Minas Gerais CEP 37200-000, Brazil
c
Biology Department, Federal University of Lavras, Lavras Minas Gerais 37200-000, Brazil
A R T I C L E I N F O A B S T R A C T
Keywords: This study evaluated the effect of cassava starch–based bionanocomposites reinforced with cellulose nanofibrils
Fragaria x ananassa Duch. obtained from oat and wheat straw as edible coatings on the maintenance of postharvest strawberry quality
Softening enzymes during refrigerated storage. The coated strawberries were compared with uncoated strawberries stored in a
Browning index
sealed polyamide package and package with rigid polypropylene lids (control). The fruits were stored at 2 ± 1◦ C
Resveratrol
Vanillin
and evaluated every 3 days over 21 days for atmospheric modification, respiratory rate, mass loss, pH, titratable
Fungal growth acidity, soluble solids, color, firmness, and cell wall enzymes, antioxidant activity, phenolic profile, and
microbiological growth. The barrier properties of the coatings promoted a lower respiratory rate and slower fruit
metabolism, delaying and minimizing events related to senescence, such as degradation of soluble solids and
organic acids, tissue browning, synthesis of anthocyanins, the activity of softening enzymes, production of
compounds with antioxidant activity, vanillin and resveratrol synthesis, and fungal growth. The coating with the
bionanocomposites maintained the quality of strawberries under refrigerated storage, indicating that this ma
terial is a biodegradable alternative to conventional package used for fruits and vegetables postharvest.
1. Introduction propensity to the attack of microorganisms, softening and, conse

quently, physical injury, among other events involved in the senescence
Strawberry (Fragaria x ananassa) is a highly consumed and appreci and postharvest deterioration of strawberries (Feliziani and Romanazzi,
ated fruit due to its sensory characteristics and nutritional appeal, being 2016; Paniagua et al., 2017; Petrasch et al., 2019).
a source of vitamin C, amino acids and compounds with antioxidant Adequate refrigeration of strawberries, between 0 ◦ C - 4 ◦ C, allows
activity (Battino et al., 2019; Mazzoni et al., 2020; Miller et al., 2019). for extending their shelf life by a few days, or even weeks (Gol et al.,
Among small fruits, it is the second most produced, second only to 2013; Perdones et al., 2012). However, it must be combined with one or
grapes (Bodelón et al., 2013; Kumar et al., 2014). Data from the Food more preservation techniques, in order to optimize its effects on pre
and Agriculture Organization of the United Nations (FAO, 2021) pointed serving the quality of the fruit. Packages that promotes atmospheric
to a total world production of 8,885,028 tons in the year 2019. modification is an important ally of refrigeration in extending the shelf
Despite all the nutritional and commercial appeal, strawberries tend life and maintaining the quality of strawberries (Giannoglou et al., 2021;
to present serious postharvest problems, exhibiting reduced shelf life Nasrin et al., 2017; Peretto et al., 2014). Nevertheless, the use of
and fast deterioration in storage; maintaining the postharvest quality of petroleum-based materials as the package has been discouraged due to
these fruits has been a major challenge for researchers (Lu et al., 2018). the impacts caused to the environment (Nascimento et al., 2018;
Because it is a non-climacteric fruit, strawberries are harvested during Nechyporchuk et al., 2016), which increasingly stimulates studies
ripening, the final stage of maturation, a period of intense metabolic involving the application of biodegradable-based materials in the post
activity; this, combined with their extremely thin tissue, increases the harvest of fruits and vegetables (Han et al., 2018; Khalil et al., 2018;
* Corresponding author.
E-mail address: [email protected] (E.V.B.V. Boas).
https://doi.org/10.1016/j.scienta.2022.111668
Received 5 May 2022; Received in revised form 7 October 2022; Accepted 30 October 2022
Available online 12 November 2022
0304-4238/© 2022 Elsevier B.V. All rights reserved.
R. Carvalho do Lago et al. Scientia Horticulturae 309 (2023) 111668
Mohamed et al., 2020; Tahir et al., 2019). This type of material is usually studies of mechanical and barrier properties, and these were the con
made with low-cost and not scarce raw materials, such as proteins, centrations that obtained the best performances (Lago et al., 2021,
lipids, and polysaccharides (Galgano et al., 2015; Kwak et al., 2021; 2020). A brief characterization of the bionanocomposites is presented in
Rhim et al., 2013). Table 1. Note that the films obtained with single cassava starch were also
Regarding applications in strawberries, polysaccharides stand out, previously characterized, but, because they presented inferior properties
with most studies concentrating on chitosan-based biopolymers (Luk to the films added CNF, they were not considered for the application test
siene and Buchovec, 2019; Muley and Singhal, 2020; Wang et al., 2020), with strawberries. The CNF’s were obtained by alkaline treatment with
even though a considerable amount of research also involves the use of NaOH and subsequent defibrillation in a microfibrillator, according to
starch-based biopolymers (Garcia et al., 2012; Pinzon et al., 2020; Lago et al. (2021, 2020).
Thomas et al., 2016).
Starch is a polysaccharide of wide occurrence in nature and can be 2.3. Fruit coating
extracted from various sources production cost (López-Córdoba et al.,
2017; Owi et al., 2019; Pelissari et al., 2018, 2017). Starch-based bio Once harvested, the strawberries were immediately taken, in
composites exhibit good gas barrier properties in the headspace refrigerated transport, to the Pilot Plant of Minimal Vegetable Process
(Sharma et al., 2019; Thakur et al., 2019), and are therefore effective in ing of the Food Science Department (DCA) of the Federal University of
promoting a modified atmosphere for the preservation of fruits, espe Lavras (UFLA) - Lavras-MG. Initially, the fruits were sanitized with so
cially those with intense respiration rate, such as strawberries. However, dium hypochlorite solution (50 ppm) for 15 min. The fruits were drained
they tend to exhibit poor mechanical properties, in addition to high at room temperature and then divided into four groups, according to the
hydrophilicity (Seligra et al., 2016; Thakur et al., 2019), which may treatments (Fig. 1(d)): fruits coated with cassava starch and oat straw
limit their use as an edible coating on strawberries, due to the high nanofibrils solution (ECOSN); fruits coated with cassava starch and
humidity and water activity presented by the fruits. Alternatives that wheat straw nanofibrils solution (ECWSN); uncoated fruits packed in
combine two or more materials, with different properties, seem to polyamide sealed package (PA) and control fruits, those without coating
mitigate the problem. An example is a use of cellulosic nanofibrils packed in polypropylene rigid package with snap-on lid. Like the control
(CNF’s), which have been proven to increase the mechanical properties fruits, the coated fruits were packed in polypropylene packages. This
and decrease the hydrophilicity of biopolymers (Rajinipriya et al., 2018; package was considered a control because it does not exert a barrier to
Xu et al., 2020); in addition, CNF’s are also extracted from renewable gas permeation in the headspace, thus not promoting atmospheric
sources, meeting the concept of sustainability. modification.
In previous studies by our research group (Lago et al., 2021, 2020), The fruits were coated by immersion. The strawberries were
the insertion of CNF’s obtained from oat and wheat straws into cassava immersed for 1 min in the film solution and then drained until the
starch-based bionanocomposites decreased the hydrophilicity of the complete drying of the solution (about 6 h) at 18◦ C and 75% R.H. They
materials and improved their mechanical properties by increasing were hung by the peduncle in order to avoid contact with the surface and
stiffness, increasing their potential for application as an edible coating. consequent localized coating loss (Fig. 1(a)). The fruits of the other
Thus, the objective of this study was to evaluate the effect of the treatments were immersed in water and kept under the same conditions
application of cassava starch-based biodegradable coatings reinforced as the coated fruits. Afterwards, the fruits were packed in polypropylene
with CNF’s of oat straw and wheat straw on the quality of strawberries packages of 3.5 11.5 15 cm, and stored in a cold chamber at 2 ± 1◦ C and
throughout the refrigerated storage, in order to expand the biodegrad 90 ± 5% R.H. The analyses were performed every 3 days, for a period of
able alternatives for the post-harvest preservation of these fruits. 21 days.
2. Material and methods 2.4. Experimental design
2.1. Raw material acquisition A 4 × 8 factorial design was used, with four levels of the packaging
factor (ECOSN, ECWSN, PA and control) and eight levels of the evalu
The cassava starch used for the bionanocomposites preparation was ation time factor (0, 3, 6, 9, 12, 15, 18 and 21 days), in three repetitions.
acquired in the local commerce of Lavras, MG, Brazil. The sorbitol so Each repetition consisted of three packages with 100g of strawberries
lution was purchased from Dinâmica®, Piracicaba, SP, Brazil. The oat each.
and wheat straw used to prepare the nanofibrils were provided by SL
Alimentos/LTDA and by EPAMIG/Experimental Farm of Lavras, MG,
Brazil, respectively. For the experiment, freshly harvested strawberries
cv. ’San Andreas’ at maturity stage ¾ (75% red) used. The fruits were
purchased from the AP Frutas & Verduras® production unit, located in Table 1
Main parameters evaluated in cassava starch-based bionanocomposites with
Bom Repouso, MG, Brazil. At harvest, the fruits were selected according
added CNF from oat and wheat straws.
to size, ripeness stage and absence of defects. The fruits were harvested
with the peduncle. The harvest took place in the morning. The poly Material Tensile Young´s Water vapor Water
strenght Modulus permeability (WVP) solubility
amide package (20 µm) was provided by AP Frutas & Verduras ®. The
(MPa) (MPa) x 10− 6 (g mm/ KPa− 1 (%)
polypropylene packages were purchased from standard suppliers. day− 1m2)
Single 5.16 ± 292.58 ± 2.15 ± 0.54 23.43 ±

2.2. Preparation of the filmogenic solutions cassava 1.07 112.94 2.17
starch film
The filmogenic solutions were prepared according to Guimarães Film with 17.16 ± 671.18 ± 1.24 ± 0.075 23.19 ±
et al. (2015). In brief, a solution of 3% (w/v) of cassava starch in distilled 50% (w/w) 3.12 257.16 1.6
of oat
water, previously hydrated for 24h, containing 30% (the mass of the straw CNF
starch) of sorbitol, was subjected to gelatinization at 80◦ C, for 20 min, Film with 12.67 ± 585.72 ± 1.45 ± 0.13 25.87 ±
under agitation (750 rpm). From the gelatinized cassava starch solution, 30% (w/w) 2.36 42.88 1.45
two different solutions were prepared: one with the addition of 50% of wheat
straw CNF
(w/w) of oat straw CNF and another with 30% addition (w/w) of wheat
straw CNF. The concentrations of CNF’s were defined based on previous Adapted from Lago et al. (2021, 2020).
2
Fig. 1. Strawberries used in the experiment. (a) strawberries with freshly applied edible coating; (b) coated strawberries after drying of the coating; (c) visual
deteriorations on the fruit; (d) strawberries packed according to treatment. ECOSN: edible coating with oat straw nanofibrils; ECWSN: edible coating with wheat
straw nanofibrils; Control: uncoated strawberries; PA: uncoated strawberries stored in polyamide-sealed package.
2.5. Analyses 2.5.3. Color parameters

Color analysis of the strawberries was performed using a Konica
Determinations of mass loss, firmness, microstructural evaluation, Minolta CR-400 colorimeter, illuminant D65, with determination of the
respiration rate, CO2 in the heaspace, coloration, pH, soluble solids (SS), variables L*, a*, b*, chroma (C*) and hue angle. The readings were taken
titratable acidity (TA), microbiological and the counting of unfit fruits at different points in the equatorial region of the fruits. The a* and b*
were performed on the fresh fruits. The other analyses were performed values were used to calculate the browning index (BI), according to Eqs.
on the fruits previously homogenized and frozen in liquid N2 and stored (2) and (3) (Muley and Singhal, 2020).
in a freezer at -80◦ C.
100 × (x − 0.31)
BI = (2)
0.172
2.5.1. Respiration rate, CO2 in headspace and mass loss
The CO2 content was evaluated using a PBI Dansensor Checkpoint a ∗ +1.75 × L∗
9900 gas analyzer (PBI-Dansensor A/S, Ringsted, Denmark). To monitor x= (3)
5.645 × L ∗ +a ∗ − 3.021 × b∗
the CO2 content inside the packages, the probe was inserted into the lid/
liner of the packages before opening, and the value of CO2 produced was Anthocyanin content was determined according to Barcia et al.
(2012), based on the cyanidin-3-glucoside molar extinction coefficient.
obtained, in percent. For the respiration rate, samples of fruits from each
repetition (around 100 g) were placed in 500 mL glass bottles, her Five grams of frozen fruits tissue were mixed with 50 mL of acidified
ethanol (pH = 1.0). After incubation for 1 h in a dark environment, the
metically sealed, kept in the cold chamber, under the same storage
conditions, and the readings were taken after a three-hour period. The solution was filtered and read in a microplate reader (EZ Read 2000) at
535 nm. The results were expressed in mg 100 g− 1.
results were expressed in mL CO2 kg− 1 h− 1.
The mass loss of the fruits throughout time was evaluated by
2.5.4. Textural parameters
weighing in an analytical balance, considering the initial mass of the
fruits (time 0) and the mass of the fruits in the evaluated storage time The firmness of the fruits was evaluated by puncture test, with the
aid of a Magness - Taylor penetrometer, using a 5 mm diameter probe.
(Eq. (1)). Exclusive packages were used for the analysis, always
weighing the same samples at each evaluation time. The puncture was made in the equatorial region of the fruits and the
results expressed in N.
Mass loss (%) =
Im − Fm
× 100 (1) The activities of the softening enzymes polygalacutornase (PG),
Im pectinamethylesterase (PME), β-galactosidase (β-gal), and cellulase (Cx)
Where: Im: initial mass (time 0); and Fm: final mass (corresponding were evaluated. For this purpose, an enzyme extract was prepared ac
to each evaluated storage time). cording to Wang et al. (2020). Eight grams of the frozen tissue was
mixed with 8 mL of 50 mmol L− 1 Tris-HCl buffer (pH= 7.0) and sub
2.5.2. TA, pH and SS jected to centrifugation (12,000 x g, 4◦ C) for 30 min. The supernatant
The titratable acidity of the fruits was determined by titration with (crude extract) was collected and stored at 4◦ C until analysis. The pro
0.1M NaOH solution, using phenolphthalein as an indicator; the pH was tein content of the enzymatic extract was determined according to the
measured in a potentiometer (Tecnal TEC-3MP) and the soluble solids Bradford technique (1976). The enzymatic activity, for the four en
content was determined by refractometry in a digital refractometer zymes, was expressed in U g− 1 protein h− 1. The unit of enzymatic ac
(Atago PAL-1, Tokyo, Japan) (AOAC INTERNATIONAL, 2016). tivity (U) was defined as the amount of enzyme capable of releasing 1
µmol of galacturonic acid (PG), carboxylic groups (PME), nitrophenol
(β-gal.) or reducing sugars (Cx). Readings were performed in a
3
microplate reader (EZ Read 2000) in triplicate. solution. After centrifugation for 8 min at 4◦ C and 7,195 x g, the su
For PG determination, the methodology of Wang et al. (2020) was pernatant was removed and considered the extract. One hundred mi
used, with minor modifications. Aliquots of 0.5mL crude extract were croliters of the extract were combined with 186 µL of 0.1% (w/v) 2,
combined with 1.0 mL of 50mmol L− 1 acetate buffer (pH= 5.5) con 6-di-chlorophenol indophenol (DFI) dye and, after 3 min incubation in
taining 0.5% (w/v) polygalacturonic acid as substrate. A control was a dark environment, a reading at 518 nm was performed. The results
made for each sample using acetate buffer instead of substrate. After were compared with an analytical curve of ascorbic acid (20 µg -100 µg)
incubation at 37◦ C for 1 h, 1.5 mL of DNS solution (1% 3.5 dini and expressed as mg ascorbic acid 100 g− 1.
trosalicylic acid and 30% potassium sodium tartrate in 0.4 mol L− 1 Extracts for the total phenolics and antioxidant activity determina
NaOH) was added to the mixtures. The reaction was stopped by adding tion were prepared according to Zitha et al. (2021), with some modifi
the tubes to a boiling water bath for 5 min after the incubation period. cations. Briefly, 2.5 g of frozen fruit tissue was mixed with 10 mL of 50%
After cooling to room temperature, 25 mL of distilled water was added to (v/v) methanol and subjected to ultrasonic bath (4◦ C, for 1 h.). The
the tubes and readings were taken at 540 nm. solution was then centrifuged at 25,400 x g for 15 min at 4◦ C. The su
The PME activity was determined according to Verma et al. (2015). pernatant was reserved and the residue was re-extracted with 10 mL of
Fifteen milliliters of 0.15 M NaCl solution containing 0.25% (w/v) citric 70% (v/v) acetone under the same conditions. At the end of the process,
pectin was added to 200 µL of the enzyme extract. The volume was made the supernatants resulting from the two extractions were combined,
up to 30 mL with distilled water and the pH adjusted to 8.0 with 0.1 M constituting the extract.
NaOH. After incubation at 30◦ C for 1 h, the solutions were titrated with For total phenolics determination, the Fast blue method was used
0.1 M NaOH until color turn, using phenolphthalein as indicator. The (Medina, 2011). Briefly, 20 µL of 0.01% (w/v) Fast Blue diazonium salt
volume of NaOH used in the titration was noted and used for calculation, was added to 200 µL of the extract in microplates. After adding another
according to Eq. (4). 20 µL of 5% NaOH, the solutions were incubated for 1 h in a dark
environment. Reading was then performed at 420 nm. The results were
(mL NaOH) × (molarity NaOH) × (1000)
PME (units mL − 1) = (4) compared to an analytical gallic acid curve (20 µg - 400 µg) and
expressed as mg gallic acid 100 g− 1.
(time (h)) × (sample volume (mL))
The β-gal. activity was determined according to Wang et al. (2020). For the evaluation of phenolic profile, extracts were prepared ac
One milliliter of acetate buffer (pH = 5.5) containing 0.5% (w/v) cording to Cunha et al. (2021). Briefly, 2.5g of sample were mixed with
p-nitrophenyl-β-D galactopyranoside was added to 1mL of the enzyme 20 mL of HPLC grade 70% (v/v) methanol and incubated for 1 h in an
extract. After incubation at 37◦ C for 30 min, the reaction was stopped by ultrasonic bath at room temperature. The obtained extract was centri
adding 0.2 mol L− 1 Na2CO3 solution. The absorbance of the solutions fuged (25,406.55 x g, 4◦ C) for 15 min and then filtered on filter paper
was measured at 400 nm. with 14µm porosity. For sample injection, the extracts were filtered
Finally, Cx activity was determined combining 1.5 mL of sodium again using 0.45 µm porous membrane filters. The quantification and
carboxymethyl cellulose (CMC) solution (10 g L− 1 in acetate buffer (pH identification of the phenolic compounds were performed in a Shimadzu
= 5.5)) and 0.5 mL of the enzyme extract. The procedure adopted was model high performance liquid chromatograph (HPLC-DAD/UV-Vis)
the same as for PG determination using DNS (Wang et al., 2020). In this (Shimadzu Corporation, Kyoto, Japan). The phenolic compounds were
case, the control consisted of 0.5 mL of enzyme extract subjected to detected at 280 nm and identified by comparison of retention times with
boiling water bath for 5 min. external standards (gallic acid, catechin, chlorogenic acid, caffeic acid,
To prepare the extracts for the soluble pectin content determination, ferulic acid, vanillin, tans-cinnamic acid, m-coumaric acid, p-coumaric
the method proposed by McCready and McComb (1952) was followed. acid, o-coumaric acid, and resveratrol). The results were expressed as
In brief, 5 g of the frozen tissue were mixed with 45 mL of 95% (v/v) mg of phenolic compound 100g− 1 of sample.
ethanol and submitted to stirring for 1 h. After overnight resting, the The antioxidant activity of strawberries was evaluated by three
contents were filtered on filter paper and washed with 2 × 50 mL of 95% different methods, β-carotene/linoleic acid system (Zitha et al., 2021),
(v/v) ethanol. The residue of the filtrations was combined with 50 mL Ferric reducing antioxidant power (FRAP) (Jiao et al., 2019) and ABTS
distilled water, stirred again for 1 h and filtered, constituting the extract. (Zitha et al., 2021), with minimal modifications.
The soluble pectin content was determined according to the Blu For the β-carotene/linoleic acid system, 50 µL of β-carotene/chlo
menkrantz and Asboe-Hansen (1973) method. In tubes containing 1 mL roform solution (1 mg mL− 1) was combined with 40 µL of linoleic acid
of extract, 3 mL of sulfuric acid/sodium tetraborate solution (0.125 M) and 530 µL of Tween 40 and dissolved in 1 mL of chloroform. The
was added in an ice bath. After 10 min of boiling in a water bath and chloroform was then completely removed from the solution by evapo
subsequent cooling in an ice bath, 100 µL of carbazole was added and the ration in an oxygenator, and the resulting mixture was diluted in
tubes were brought back to a boiling water bath for 15 min. After oxygenated water to an absorbance of 0.6 - 0.7 at 470 nm, obtaining the
cooling in an ice bath, the tubes were read at 530 nm. β-carotene/linoleic acid system solution. Then, aliquots of 270 µL of the
For microstructural analysis, samples of the strawberry tissues were system solution were added in microplates containing 20 µL of the
removed at each evaluation time using slides and inserted in microtubes antioxidant extracts of the samples, being read at 470 nm, obtaining the
containing modified Karnovsky fixative, and kept until the moment of values of initial absorbance (Initial Abs.). After incubation for 2 h in a 40
sample preparation. For the preparation of the specimens, the samples ◦
C water bath, the second reading was performed, obtaining the final
were fractured in liquid nitrogen and subjected to dehydration in absorbance values (Final Abs.). The % inhibition of β-carotene discol
acetone gradient, followed by drying in a Critical point apparatus (Bal- oration (% protection) was then calculated according to Eqs. (5) and (6).
Tec). Then, the specimens were mounted on stubs, submitted to metal
(Initial Abs. − Final Abs.)sample × 100
lization in a gold evaporator apparatus (Bal-Tec) and observed under a % oxidation = (5)
(Initial Abs. − Final Abs.)system
LEO EVO 40 XVP scanning electron microscope (SEM) in the Laboratory
of Electron Microscopy and Ultrastructural Analysis (LME) of the % protection = 100 − (% oxidaç∼ao) (6)
Department of Plant Pathology at UFLA. Images obtained at the evalu
ation times 0, 12 and 21 days were used. For antioxidant activity evaluation by the FRAP method, aliquots of
9 µl of antioxidant extracts of the samples were combined with 27 µL of
2.5.5. Bioactive compounds distilled water and 264 µL of FRAP solution (containing TPTZ, ferric
The ascorbic acid content of strawberries was determined according chloride and acetate buffer). After incubation in a water bath at 37◦ C for
to Muley and Singhal (2020), with minimal modifications. Five grams of 30 min, the absorbances of the samples were read at 595 nm. The results
frozen tissue was mixed with 20 mL of 2% (w/v) metaphosphoric acid were calculated based on an analytical curve of ferrous sulfate (FeSO4)
4
(500 µM to 2000 µM) and expressed as µM of ferrous sulfate (FeSO4) g− 1. statistical software (RStudio Team, 2015).
For antioxidant activity determination by the ABTS method, the
radical solution (ABTS•+) was prepared by combining 7 mM of potas 3. Results
sium persulfate and 2.5 mM of ABTS solution, and the mixture was kept
at rest for 16 h in a dark environment and room temperature. After this After the filmogenic solution dried, the coatings adhered well to the
period, the radical mixture was diluted in ethanol to an absorbance of fruits, without any uncoated areas. Visual changes between coated and
0.70 ± 0.05 at 734 nm. Aliquots of 297 µL of the radical solution were uncoated fruits were not noted (Fig. 1(b)).
combined with 3 µL of antioxidant extract of the samples, and after 6 Variables influenced by the coating factor alone were represented by
min of reaction, reading at 734 nm was performed. The results were bar charts, comparing the means of the different types of packaging.
compared to an analytical trolox curve (0 µM - 200 µM) and expressed in Variables influenced by the storage time alone were represented by
µM trolox equivalent (TE) g− 1. scatter lines, showing the overall behavior of the averages over the time.
The assays were conducted in triplicate and readings were taken in a In the case of interaction between storage time and coating, bar charts
microplate reader (EZ Read 2000). express the behavior of the different treatments within each evaluation
time.
2.5.6. Fruit spoilage
The evaluation of fruit spoilage throughout time was performed by
microbiological analysis (Salmonella sp., total coliforms, and fungi) and 3.1. Respiratory rate, headspace CO2 and mass loss
visual determination of fruits not apt for consumption.
The presence of Salmonella sp. was verified according to the 4.12 The respiratory activity of strawberries oscillated at approximately
method (United States Department of Agriculture (USDA), 2017), with 20 mL CO2 kg− 1 h− 1 in the first 18 days of storage, rising thereafter to 45
adaptations. In brief, 2.5 g added to erlenmeyers containing 225 ml of mL CO2 kg− 1 h− 1 at 21 days (Fig. 2(a)). ECOSN and ECWSN strawberries
buffered water and incubated, at 37◦ C, for 18 h. Subsequently, sample exhibited lower respiratory rates than the control and PA strawberries.
enrichment was performed using the tetrationate and rapaport broths, A greater accumulation of CO2 was observed in the PA packages than
with incubation at 37◦ C for 24 h. Plating was performed on Hektoen in the others during storage (Fig. 2(b)). The CO2 levels in the PA pack
Enteric Agar medium followed by incubation at 37◦ C for 24 h. Suspect ages exceeded 1%, although they did not exceed 0.3% in the poly
colonies were isolated and transferred to tubes containing triple sugar propylene packages despite the fruit coating.
iron agar (TSI) and lysine iron agar (LIA), incubated at 37◦ C for 24 h and In all groups, there was an increase in fruit mass loss during storage,
subsequently submitted to biochemical tests. which reached approximately 1% on the 21st day (Fig. 2(c)).
For total coliform counts, the most probable number (MPN) 9:2015
method was used (Kornacki et al., 2015). In brief, aliquots of samples
3.2. TA, pH and SS
diluted in buffered water were inserted into tubes containing Lauryl
Sulfate Tryptose Broth (LST) in serial dilution and incubated at 35◦ C for
The TA of the strawberries decreased from 1.13 to approximately
48 h. After this period, tubes containing growth and gas production were
0.95% during the 21 days of storage, and on average, ECOSN and
submitted to the confirmative test for total coliforms: Tubes containing
ECWSN had the highest mean TA (Fig. 2(d)). The pH oscillated slightly
LST were placed in tubes containing 2% Brilliant Green Broth (GB) and
during storage, between 3.28 and 3.39 (Fig. 2(e)). ECOSN and ECWSN
incubated at 35◦ C for 48 h. After this period, the tubes with growth and
had the lowest mean pH at 0, 18, and 21 days of storage, while the
gas production were considered positive for total coliforms, being sub
highest mean pH was observed for ECOSN on storage day 6. No other
mitted to MPN counting and the results expressed in MPN g− 1.
differences were noted.
Fungal analysis corresponded to the count of molds and yeasts,
The SS content was influenced by the time × treatment interaction
determined according to the APHA 21:2015 plating method, with
(Fig. 2(f)). Small oscillations in the means were observed in the first
counting of colony forming units (CFU) (Ryu and Wolf-Hall, 2015).
storage times regardless of treatment. A slight but significant increase in
Aliquots of serial dilutions of the homogenized samples in buffered
the soluble solid content was observed in the control and PA straw
water were subjected to surface plating with dichloran rose bengal
berries on the last day of storage. Conversely, the soluble solid content of
chloramphenicol agar (DRBC) culture medium. After incubation at 25 ◦ C
the coated fruits showed a decreasing trend starting on the 12th day of
for 5 days, the numbers of typical mold colonies and typical yeast col
storage, whereas ECOSN strawberries showed a stabilization of the
onies were measured (after microscopic confirmation of cell
mean starting on the 15th day, and ECWSN strawberries showed two
morphology), and the sum was considered as total count and expressed
significant drops, at 18 and 21 days of storage. Nevertheless, the coated
in log CFU g− 1.
strawberries exhibited the highest mean soluble solid content at most
At each evaluation time, the percentage of fruits unfit for con
times.
sumption was also counted, considering the ratio between the total
number of fruits and the number of fruits with some type of visible
damage (Eq. (7)). The presence of brownish areas, softened areas and 3.3. Color changes
visible growth of fungal mycelia were considered as alterations (Fig. 1
(c)). Decreasing trends in L* and increasing trends in BI were observed
throughout strawberry storage in all groups, although this was less
Tf − If
Unfit fruits (%) = × 100 (7) pronounced in the ECOSN and ECWSN fruits (Fig. 3(a, b)). An increase
Tf
in C*, followed by a decrease, was observed in the strawberries of all
Where: Tf: total number of fruits; and If: number of fruits with visible groups (Fig. 3(c)). A decreasing trend in h◦ was observed in the ECOSN
changes. and ECWSN fruits during the 21 days of storage, while the C and PA
fruits showed a reduction in this variable, followed by an increase at the
end of storage. Control fruits had lower h◦ than the others from the 9th
2.6. Statistical analysis to the 15th day of storage (Fig. 3(d)). The levels of anthocyanins
increased during strawberry storage, more pronouncedly in the control
The data obtained were analyzed using variance test, Scott Knott’s strawberries, followed by PA (Fig. 3(e)). ECOSN resulted in a lower in
average test (P < 0.05), principal component analysis (PCA), hierar crease in anthocyanins than ECWSN until the 9th day of storage, and the
chical clustering, and Pearson’s correlation analysis, using R Studio two groups had similar levels from day 12 to day 21.
5
Fig. 2. Bar graphs and scatter lines plots for the variables respiration rate (a); CO2 in headspace (b); mass loss (c); titratable acidity (d); pH (e) and soluble solids (f) of
strawberries in different types of package stored cold for 21 days. ECOSN: edible coating with oat straw nanofibrils; ECWSN: edible coating with wheat straw
nanofibrils; Control: uncoated strawberries; PA: uncoated strawberries stored in polypropylene package sealed with polyamide. Error bars indicate standard devi
ation values. Treatments followed by the same letters (upper case for storage time and lower case for treatment) do not differ by Scott Knott test (P < 0.05).
3.4. Textural changes 18 (Fig. 4). On average, the ECOSN and ECWSN fruits were firmer and
had lower PG activity than the control and PA fruits (Fig. 4(a, b)).
A reduction in firmness and increase in the activity of PG and Cx β-Gal activity did not vary as a function of the package/coating and
enzymes and in the soluble pectin content, as well as increased PME storage time factors, having an overall mean of 0.008 ± 0.001 U g− 1
activity, were observed from days 9 to 12, followed by a drop until day protein h− 1. Differences in soluble pectin levels between treatments
6
Fig. 3. Bar graphs plots for coloration param

eters and anthocyanin content of strawberries
in different types of package stored cold for 21
days. ECOSN: edible coating with oat straw
nanofibrils; ECWSN: edible coating with wheat
straw nanofibrils; Control: uncoated straw
berries; PA: uncoated strawberries stored in
polypropylene package sealed with polyamide.
Error bars indicate standard deviation values.
Treatments followed by the same letters (upper
case for storage time and lower case for treat
ment) do not differ by Scott Knott test (P <
0.05).
were observed only after the 15th day of storage (Fig. 4(d)). The PA had flaccid structures, rugosity, and deformation in the cavities, while
package and coatings reduced the pectic solubilization of strawberries at the coated fruits still had part of the initial structure with well-preserved
15 and 21 days of storage, while ECOSN resulted in the lowest mean at cavities. Although the fruits coated with both bionanocomposites had a
18 days of storage. more structured cell wall than the other groups, ECOSN showed the least
To illustrate the textural changes in the strawberries subjected to the structural damage during storage, keeping a similar structure
different treatments, micrographs obtained by SEM at 0, 12, and 21 days throughout.
of storage are shown in Fig. 5. At the beginning of the experiment (day
0), an intact structure was observed, with well-defined cavities, 3.5. Bioactive compounds
regardless of treatment. On the 12th day of storage, a slight decrease in
the integrity of the structure was observed, with the onset of flaccidity of Reductions in the levels of ascorbic acid, as well as in the antioxidant
the cavities, which was more pronounced in the control and PA fruits. At activity measured by the FRAP and β-carotene/linoleic acid methods,
the end of the experiment (21st day of storage), the control and PA fruits were observed during the 21 days of storage of the strawberries (Fig. 6).
7
Fig. 4. Bar graphs and scatter lines

plots for the texture-related parameters
of strawberries in different types of
package stored cold for 21 days ECOSN:
edible coating with oat straw nano
fibrils; ECWSN: edible coating with
wheat straw nanofibrils; Control: un
coated strawberries; PA: uncoated
strawberries stored in polypropylene
package sealed with polyamide. Error
bars indicate standard deviation values.
Treatments followed by the same letters
(upper case for storage time and lower
case for treatment) do not differ by
Scott Knott test (P < 0.05).
The package/coating affected only the variables ascorbic acid, ABTS, means: catechin (787.65 ± 357.41 mg100 g− 1), chlorogenic acid (64.93
and FRAP. ECOSN strawberries had the highest means for these vari ± 30 mg100 g− 1), ferulic acid (44.42 ± 7.33 mg100 g− 1), p-coumaric
ables, whereas PA strawberries had the lowest. Control fruits had lower acid (7.91 ± 1.57 mg100 g− 1), m-coumaric acid (78.62 ± 18.29 mg100
mean ascorbic acid, FRAP, and ABTS than ECOSN strawberries and g− 1), and o-coumaric acid (5.40 ± 0.81 mg100 g− 1). A decrease in the
lower mean ascorbic acid and FRAP than ECWSN strawberries. gallic acid content was observed in the first 6 days of storage, followed
Reduction in total phenolic content over the 21 days of storage was by an increase over the next 6 days, with a trend toward stabilization
also observed (Fig. 7(a)). Of the 11 phenolic compounds screened, nine thereafter (Fig. 7(b)). Conversely, the resveratrol content showed an
were identified in the strawberries. Gallic acid and resveratrol were increasing trend over the 21 days of storage (Fig. 7(c)), the highest mean
affected by storage time, while vanillin and resveratrol were affected by being observed in the control fruits. The control followed by PA straw
the package/coating. The contents of the other identified phenolic berries had the highest mean vanillin content compared to the ECOSN
compounds did not vary with the factors studied, having the following and ECWSN strawberries (Fig. 7(d)).
8
Fig. 5. Micrographs obtained in SEM for strawberries in different types of package stored cold at 0, 12 and 21 days. ECOSN: edible coating with oat straw nanofibrils;
ECWSN: edible coating with wheat straw nanofibrils; Control: uncoated strawberries; PA: uncoated strawberries stored in polypropylene package sealed with
polyamide.. Magnification 350 x.
3.6. Fruit spoilage 3.7. PCA and Pearson correlation
There was no presence of Salmonella sp., and the total coliform count To summarize the main results obtained for the studied variables and
was less than 2 × 10− 3, the maximum limit allowed by current legisla visualize the interactions between them, principal component analysis
tion (BRASIL, 2001). The package/coating and storage time did not (PCA) (Fig. 9(a)), hierarchical clustering (Fig. 9(b)), and Pearson cor
affect these variables. relation (Fig. 10) were applied to the significant variables.
The spoilage of strawberries over time, represented by fungal growth Regarding the PCA plot, the two main components explained 56.66%
and the percentage of fruits unfit for consumption, was significantly of the total variation in the data. The loadings values (Table 2) indicate
affected by the treatment × time interaction (Fig. 8). There was an in that the variables PG, Cx, L*, ML, TA, anthocyanins, MY, resveratrol, SP,
crease in fungal growth during storage, regardless of treatment, UF, hue, SS, BI, RR, ascorbic acid, and firmness were responsible for the
although it was more pronounced in the control fruits and less pro variations in principal component (PC) 1, while the variables vanillin,
nounced in the coated fruits (Fig. 8(a)). C*, BI, AA, ABTS, ML, UF, ascorbic acid, CO2, Cx, SS, resveratrol and
The behavior of fungal growth was reinforced by the results of the FRAP explained the variations in PC2. The hierarchical cluster analysis
percentage of fruits unfit for consumption (Fig. 8(b)). The control separated the treatments into two large groups (clusters), the first cor
strawberries showed visible spoilage as early as day 12, while the first responding to the coated treatments at days 0 and 3 and the second
visible spoilage was only observed on day 15 for PA fruits and day 18 for corresponding to the other treatments. Within the second cluster,
coated fruits. The percentage of unfit fruits was significantly higher in several subgroups formed. The strawberries coated with ECOSN and
the control strawberries after 15 days of storage. Lower mean percent ECWSN were separated into subgroups according to storage time. The
ages of unfit fruits at 18 and 21 days of storage were observed in the subgroups formed by these treatments at 6, 9, 12, and 15 days of storage,
ECOSN fruits than in the ECWSN and PA fruits. together with the treatments corresponding to the first cluster (days
9
Fig. 6. Bar graphs and scatter lines plots for the ascorbic acid content and antioxidant activity of strawberries in different types of package stored cold for 21 days
ECOSN: edible coating with oat straw nanofibrils; ECWSN: edible coating with wheat straw nanofibrils; Control: uncoated strawberries; PA: uncoated strawberries
stored in polypropylene package sealed with polyamide. Error bars indicate standard deviation values. Treatments followed by the same letters (upper case for
storage time and lower case for treatment) do not differ by Scott Knott test (P < 0.05).
0 and 3), occupied the first quadrant (Q1) in the PCA plot and were with the variables PG, MY, SP, resveratrol, Cx, RS, WL, and IF. The
characterized by the highest SS, TA, hue angle, L* value, ascorbic acid, control treatments at days 18 and 21 also formed two other distinct
and antioxidant activity. The correlations became weaker (treatments subgroups, indicating even stronger correlations with these variables.
more distant from the corresponding vectors) as the storage time pro Considering the correlation plot, all the variables besides CO2, C*,
gressed. The coated strawberries in the last storage times (days 18 and and PME showed significant correlations with each other. The patterns
21) formed a subgroup located in Q4, characterized by the parameters observed in the correlation plot can be referenced to reinforce the dis
PG, MY, SP, resveratrol, Cx, RR, WL, and UF. Within this same subgroup, cussion of the data, presented next.
ECOSN T18 stood out, forming another isolated subgroup that was more
distant from these variables than any other was. The control and PA 4. Discussion
treatments at day 0 formed an isolated subgroup, with weak correlations
between the variables. The treatments PA at days 3 to 9 and control at 4.1. Respiratory rate, headspace CO2 and mass loss
day 3 formed a subgroup, characterized by the C* and PME values (Q2).
Q3 was characterized by the variables vanillin, CO2, BI, anthocyanins, Although strawberries are classified as non-climacteric, increases in
and respiratory rate, in which the treatments control at days 6 to 15 and respiratory activity in ripe strawberries have been reported (Tosetti
PA at days 12 and 15 formed a subgroup. The control and PA treatments et al., 2020), as was also observed in the present study. This increase has
at days 18 and 21 formed another subgroup, which showed correlations been associated with ethylene, whose biosynthesis is high at the
10
Fig. 7. Bar graphs and scatter lines plots for the total phenolic and phenolic profile of strawberries in different types of package stored cold for 21 days ECOSN: edible
coating with oat straw nanofibrils; ECWSN: edible coating with wheat straw nanofibrils; Control: uncoated strawberries; PA: uncoated strawberries stored in
polypropylene package sealed with polyamide. Error bars indicate standard deviation values. Treatments followed by the same letters (upper case for storage time
and lower case for treatment) do not differ by Scott Knott test (P < 0.05).
advanced ripeness stages of strawberries (Sánchez-Sevilla et al., 2017). times higher than the polypropylene package. In fact, the low levels of
Starch-based coatings have been demonstrated to be effective as a bar CO2 observed in the polypropylene package group, regardless of
rier against atmospheric gases (Sharma et al., 2019; Thakur et al., 2019), whether the packed strawberries were coated, were due to the closure
and the incorporation of nanofibrils tends to augment the barrier system of the package, that is, the fitting. The fitting of the lid allows
properties, decreasing gas permeability. Thus, the lower respiratory rate respiratory gases to permeate while minimally impacting the accumu
exhibited by ECOSN and ECWSN fruits might be linked to the barrier lation of CO2. Conversely, the PA package was sealed, restricting gas
properties of the coatings. By minimizing O2 permeation, the coatings exchange to the film’s permeability under storage conditions. However,
can decrease respiratory activity, directly by limiting the substrate the accumulation of CO2 even in the PA package, just above 1%, is
available for O2 respiration or indirectly by reducing the synthesis of considered low, having little potential to impact the fruit physiology.
ethylene, a phytohormone that increases respiration. The higher respi The small atmospheric modification generated by the PA package was
ration rate observed in control and PA fruits can also be attributed to the due to the low temperature at which the fruits were stored, which was
higher microbial growth observed in these treatments, mainly control, sufficient to keep their respiratory activity low, resulting in a small
compared to the coated strawberries. In this case, the production of CO2 accumulation of CO2 in the headspace.
as an end product of the respiration of molds and yeasts may have Mass loss is frequently reported during strawberry storage; these
influenced the measured values. The positive correlation shown be fruits are highly susceptible to rapid water loss due to their extremely
tween microbial growth (MY) and respiration rate (RR) (Fig. 10) re thin peel, making for a low barrier to water vapor (Luksiene and
inforces the hypothesis. Buchovec, 2019). Nevertheless, the average mass loss of the fruits was
The PA package resulted in an accumulation of CO2 approximately 3 only approximately 1% on the 21st day of storage. Strawberry mass
11
Fig. 8. Bar graphs and scatter lines plots for the variables molds and yeasts (a) and % unfit fruits (b) of strawberries in different types of package stored cold for 21
days. ECOSN: edible coating with oat straw nanofibrils; ECWSN: edible coating with wheat straw nanofibrils; Control: uncoated strawberries; PA: uncoated
strawberries stored in polypropylene package sealed with polyamide. Error bars indicate standard deviation values. Treatments followed by the same letters (upper
case for storage time and lower case for treatment) do not differ by Scott Knott test (P < 0.05).
Fig. 9. Principal component analysis (PCA) (a) and hierarchical clustering (b) of the variables evaluated in strawberries in different types of package stored in cold
storage for 21 days. SS: soluble solids; TA: titratable acidity; MY: molds and yeasts; UF: unfit fruits; ML: mass loss; RR: respiration rate; BI: browning index; SP: soluble
pectin; PG: polygalacturonase; PME: pectinamethylesterase; Cx: cellulase; AA β-carot. /lin.acid: antioxidant activity β-carotene/linoleic acid method; AA FRAP:
antioxidant activity FRAP method; AA ABTS: antioxidant activity ABTS method; TP: total phenolics; GA: gallic acid. ECOSN: edible coating with oat straw nanofibrils;
ECWSN: edible coating with wheat straw nanofibrils; PA: strawberries stored in polyamide-sealed package. Circled treatments in the PCA plot correspond to the main
subgroups formed in the hierarchical clustering analysis.
losses well above this value have been reported, ranging from 16% to the fruit tissue and the surrounding air (Jiang et al., 2020), the behavior
40% in strawberries with different types of coatings, and may reach 50% observed was expected. Fig. 10 shows a positive correlation between the
in uncoated fruits stored for 8 to 15 days at 5◦ C (Muley and Singhal, strawberry mass loss and respiratory rate.
2020; Treviño-Garza et al., 2015) or 7 days at 24◦ C (Kwak et al., 2021).
The substantially lower mass loss values observed in the present study
4.2. pH, TA, and SS
may be due to the lower storage temperature used (2 ± 1◦ C), as well as
the high relative humidity of storage (95 ± 2%). Since mass loss is a
The decrease in TA during fruit storage can be attributed to the use of
function of the respiratory rate and the evaporation of moisture between
organic acids as a substrate for respiration and as a carbon skeleton for
12
Table 2
PCA loadings.
Variable PC1 PC2
CO2 0.31 -0.39*

pH 0.47 -0.03
SS -0.76* 0.35*
TA -0.84* -0.07
MY 0.79* 0.16
UF 0.78* 0.43*
ML 0.85* 0.44*
RR 0.74* -0.03
Anthocyanins 0.83* -0.04
L* -086* -0.01
C* -0.39 -0.69*
hue -0.78* 0.06
BI 0.74* -0.54*
Firmness -0.67* 0.26
SP 0.79* 0.32
PG 0.89* 0.12
PME -0.03 -0.22
Cx 0.86* 0.36*
AA β-car./Lin.acid -0.47 -0.03
AA FRAP -0.65 0.35*
AA ABTS -0.4 0.50*
Ascorbic acid -0.69* 0.42*
TP -0.63 0.19
GA -0.38 0.33
Fig. 10. Correlation graph for the variables evaluated in strawberries in Vaniliin 0.34 -0.78*
different types of package stored in cold storage for 21 days. SS: soluble solids; Resveratrol 0.79* 0.35*
TA: titratable acidity; MY: molds and yeasts; UF: unfit fruits; ML: mass loss; RR:
respiration rate; BI: browning index; SP: soluble pectin; PG: polygalacturonase; Averages marked with * indicate significant correlation with PC (P < 0.05). SS:
PME: pectinamethylesterase; Cx: cellulase; AA β-carot. /lin.acid: antioxidant soluble solids; TA: titratable acidity; MY: molds and yeasts; UF: unfit fruits; ML:
activity β-carotene/linoleic acid method; AA FRAP: antioxidant activity FRAP mass loss; RR: respiration rate; BI: browning index; SP: soluble pectin; PG:
method; AA ABTS: antioxidant activity ABTS method; TP: total phenolics; GA: poligalacturonase; PME: pectinametilesterase; Cx: celulase; AA β-carot./lin.acid:
gallic acid. Blue coloration indicates positive correlations and red coloration, antioxidant activity β-carotene/linoleic acid method; AA FRAP: antioxidant
negative correlations. The size of the spheres and the intensity of the staining activity FRAP method; AA ABTS: antioxidant activity ABTS method; TP: total
are proportional to the degree of correlation. Areas highlighted with X indicate phenolics; GA: gallic acid.
non-significant correlation (P > 0.05).
correlation between both variables. The browning of the surface of
the synthesis of new substances during storage. In fact, the ECOSN and strawberries can be attributed to two events. First, it may be associated
ECWSN fruits, which had the highest mean TA, exhibited lower respi with the enzymatic browning process, in which the enzyme polyphenol
ratory rates, which is in agreement with this hypothesis. This finding is oxidase (PPO) oxidizes phenolic compounds present in fruits to o-qui
further reinforced by Fig. 10, which shows a negative correlation be nones, culminating in the production of brownish pigments, the mela
tween TA and respiratory rate. Conversely, a positive correlation was nins (Constabel and Barbehenn, 2008; Queiroz et al., 2008). A high
observed between TA and total phenolics. Phenolic compounds have an correlation between BI and polyphenol oxidase activity has been re
acidic character that contributes to the acidity of fruits. Thus, the ported (Ali et al., 2015). Second, the browning of the fruits may be
degradation of phenols during storage may be another explanation for related to the action of fungi that cause tissue darkening (Feliziani and
the decrease in TA in these strawberries. Tosetti et al. (2020) demon Romanazzi, 2016; Higuera et al., 2019). The positive correlation be
strated that malic acid degradation, and consequent increase in pH, are tween BI and fungal growth (Fig. 10) reinforces this hypothesis.
linked to the senescence of strawberries. Thus, the fact that the coated Thus, the lower BI exhibited by the coated strawberries can be
fruits had the lowest mean pH values in the last two storage times (18 attributed to the indirect effects of the edible coatings. By exerting a
and 21 days), the same period in which the lowest overall means for TA barrier effect and limiting the respiratory rate and thereby fruit meta
were observed, may indicate lower consumption of organic acids in bolism, the coatings delayed senescence events related to the loss of fruit
these treatments, which reinforces the effectiveness of the coatings quality, as seen thus far and as will be discussed below. Among these
applied as regulators of catabolic events that culminate in the loss of events, firmness loss can be highlighted. It has an indirect relationship
strawberry quality. with enzymatic browning. The decompartmentalization of membranes,
The decrease in SS over the storage time can be attributed to its one of the causes of firmness loss, allows contact between isoforms of
consumption as a substrate in fruit respiration, in addition to possibly polyphenol oxidases and peroxidases and their phenolic substrates,
being related to fungal attack (Siedliska et al., 2018). Fig. 10 shows resulting in browning. This statement is reinforced by the negative
negative correlations between SS, respiratory rate, and fungal growth, correlation between the BI and firmness parameters, in addition to the
which reinforces this hypothesis. A strong negative correlation was also positive correlation between BI and SP, PG, and Cx, parameters related
observed between SS and anthocyanin content. This may be indicative of to fruit softening (Fig. 10). In addition, the coatings used may have
glucose consumption during anthocyanin synthesis (Sasaki et al., 2014). reduced the permeation of O2 from the environment into the strawberry
Since the coated strawberries exhibited the highest mean SS most of the tissues, reducing the activity of enzymes that use this atmospheric gas as
time, the coatings seemed to have a positive effect on the containment of a substrate.
the metabolic processes related to the degradation of these compounds. Finally, considering the hypothesis of tissue darkening from the ac
tion of fungi, the lower BI values presented by the coated strawberries
4.3. Color changes can be attributed to the effect of the coatings on the observed deceler
ation in fungal growth.
The reduction in the L* value of the fruits indicates their darkening, The decrease in h◦ , visually noted by the increase in the red color of
corroborated by the increase in the BI and the strong negative the strawberries, is related to the synthesis of anthocyanins, which is
13
confirmed by the negative correlation between both variables (Fig. 10). of cell integrity in the coated strawberries.
Anthocyanins are synthesized by the phenylpropanoid pathway during
natural ripening and can be considered a response to physiological stress 4.5. Bioactive compounds
and metabolic disorders related to fruit senescence (Ma and Constabel,
2019; Sharma et al., 2019). In fact, positive correlations were observed The reductions in ascorbic acid, total phenolics, and antioxidant
between anthocyanin content and fungal growth, percentage of unfit activity observed in the strawberries irrespective of the package/coating
fruits, mass loss, respiratory rate, BI, soluble pectin, and activity of the may have been associated with common redox reactions during fruit
softening enzymes PG and Cx, whereas their level was negatively ripening and senescence. Throughout the aging of fruits, free radicals
correlated with SS, TA, firmness, ascorbic acid and total phenolic con are formed and scavenged by the antioxidants present, such as ascorbic
tent, and antioxidant activity. These results reinforce the hypothesis acid and phenolic acids, which culminates in the reduction in these
that, in the present context, the increase in anthocyanins was related to compounds and in antioxidant activity. The very oxidation of phenolic
senescence events in strawberries. The lower anthocyanin accumulation compounds can be reversed by the reducing action of ascorbic acid,
observed in the coated strawberries suggests the efficacy of the coatings which is reversibly converted to dehydroascorbic acid, both compounds
in delaying senescence. having vitamin C activity. However, if dehydroascorbic acid is oxidized,
the activity of vitamin C is completely and irreversibly lost. The oxida
4.4. Textural changes tion of mono- and dihydroxy phenols to o-quinones can therefore be
reversed by vitamin C (Ali et al., 2015; Landi et al., 2013). If o-quinones
The increase in PME activity concomitant with the onset of PG in polymerize, they give rise to melanins, which are responsible for
crease suggests the importance of partial demethylation of the pectic browning. This may be the explanation for the strong negative corre
chain for the depolymerizing action of PG. The activities of the PG and lation between BI and ascorbic acid content (Fig. 10).
Cx enzymes showed a negative correlation with firmness and a positive The effect of the applied coatings on reducing the loss of ascorbic
correlation with the soluble pectin content (Fig. 10), which demon acid and antioxidant activity in strawberries may be related, among
strates the role of these enzymes, direct in the case of PG and indirect in other aspects, to the barrier properties exhibited by these materials.
the case of Cx, in the depolymerization and solubilization and softening According to Yaman and Bayoindirli (2002), the oxidation of ascorbic
of strawberries. Indeed, PG is one of the most abundant enzymes in acid can be attributed to the action of the enzymes phenol oxidase and
ripening strawberries and is associated with their softening (Moya-León ascorbic acid oxidase, whose activities depend on the O2 content in the
et al., 2019; Wang et al., 2020). The absence of significant correlations medium. Jiao et al. (2019) attributed the preservation of ascorbic acid
between PME activity and other variables indicates that the enzyme content in peaches coated with a chitosan–chlorogenic acid conjugate to
exerted an indirect effect on cell wall disintegration, whereas PG and Cx the inhibition of respiratory rate. The same was reported by Trevi
were the determining enzymes for firmness loss in strawberries. ño-Garza et al. (2015) and Gol et al. (2013) for strawberries coated with
The coatings were effective at limiting the increase in PG activity and chitosan. In fact, the higher the respiratory rate, the faster the fruit ages,
softening of the strawberries during storage. Thus, considering the high increasing the chances of free radical formation and consumption of its
negative correlation of PG with strawberry firmness, we can infer that natural antioxidant arsenal. This explains the negative correlation
the coatings applied contributed to the deceleration of the processes observed between ascorbic acid and the respiratory rate of the straw
involved in softening. Considering that softening mediated by enzymes berries (Fig. 10). Therefore, due to the possible barrier imposed on O2
is related to metabolic activity and fruit senescence, the effect exerted by and the demonstrated reduction in the respiratory activity of the fruits,
the coatings on the respiratory rate may explain their performance in the coatings with ECOSN and ECWSN reduced the losses of ascorbic acid
delaying strawberry softening. In fact, there was a negative correlation and antioxidant activity during the storage of strawberries.
between respiratory rate and fruit firmness, in addition to positive cor Gallic acid has been reported as a natural antioxidant, acting against
relations between respiratory rate and SP, PG activity, and Cx activity endogenous oxidation reactions in fruits (Polewski et al., 2002; Yen
(Fig. 10). Although the package/coating and storage time factors did not et al., 2002). The degradation of gallic acid, as occurred for the total
affect β-gal, this enzyme was active in the strawberries studied, which phenolic content, could be attributed to the senescence events of
does not rule out its importance in the ripening of these fruits. strawberries, although this compound was not affected by the pack
In addition to the action of these enzymes, other events related to age/coating. In fact, the gallic acid content showed a negative correla
senescence may have led to the firmness loss in the strawberries, such as tion with parameters such as fungal growth, percentage unfit fruits,
fungal development. As observed in Fig. 10, the growth of molds and mass loss, respiratory rate, BI, soluble pectin, and PG and Cx activity,
yeasts had a negative correlation with firmness and a positive correla while a positive correlation was found for SS, TA, firmness, ascorbic acid
tion with the soluble pectin content. In fact, many fungal species that content, and antioxidant capacity by the three methods used (Fig. 10).
affect strawberries can produce pectinolytic and cellulolytic enzymes, The synthesis of resveratrol, observed in the strawberries studied
which degrade fruit tissue, culminating in firmness loss. Examples are here, can also be associated with senescence. The enzyme
R. stolonifer, Mucor spp., and B. cinerea, fungi related to the development phenylalanine-ammonia-lyase, the main enzyme responsible for antho
of soft rot and gray mold in strawberries, and pathologies that culminate cyanin synthesis, which occurs during strawberry ripening and senes
in tissue softening (Feliziani and Romanazzi, 2016; Petrasch et al., 2019; cence, plays an important role in resveratrol synthesis (Giovinazzo et al.,
Romanazzi et al., 2013). Thus, the protection of the applied coatings 2012). The positive correlation between resveratrol and anthocyanin
against fungal growth may be another explanation for the lower firm levels (Fig. 10) may explain the association between resveratrol accu
ness loss in these groups. mulation and senescence. Acceleration of the respiratory rate, the ac
The correlation plot (Fig. 10) also indicates an inverse relationship tions of degrading enzymes, and fungal growth are events involved in
between strawberry firmness and BI. Areas affected by enzymatic the senescence of fruits such as strawberries (Dixon and Paiva, 1995;
browning have been associated with a greater propensity to cell integ Vogt, 2010). Resveratrol synthesis is stimulated as a response to these
rity loss (Franck et al., 2007). While the loss of membrane integrity can events (Krawczyk, 2019; Li et al., 2017; Lizard et al., 2020; Feliziani and
optimize enzymatic browning via enzyme-substrate contact, as dis Romanazzi, 2016; Petrasch et al., 2019; Xu et al., 2018). In fact, the
cussed above, enzymatic browning may also be related to firmness loss. correlation plot (Fig. 10) shows that the resveratrol content was posi
These results indicate how the evaluated variables are closely inter tively correlated with the respiratory rate, fungal growth, percentage of
connected and how the coatings had indirect effects on them. unfit fruits, mass loss, BI, pectin, and PG and Cx activity, while negative
The micrographs shown in Fig. 6 corroborate the results found for correlations were observed for firmness, antioxidant activity, and
firmness and softening enzyme activity, indicating greater preservation ascorbic acid content. Given that the coated fruits had lower mean
14
resveratrol content than control fruits, ECOSN and ECWSN seem effi contribution of the evaluated variables to the loss of strawberry quality
cient at delaying and attenuating the events involved in senescence and and highlights the effectiveness of the applied coatings on delaying these
metabolic disorders in strawberries. events.
Vanillin has been associated with the lignification of stressed and
injured plant tissues and is produced from the oxidation of ferulic acid 4.7. PCA and Pearson correlation
(Kumar and Pruthi, 2014). Thus, the higher vanillin content observed in
the control strawberries may be indicative of greater tissue damage in The PCA (Fig. 9(a)) and hierarchical clustering (Fig. 9(b)) plots
these fruits due to senescence events, such as increased respiratory rate, reinforce what was discussed, showing that the coated fruits maintained
enzymatic browning, and the activity of softening enzymes, and fungal the highest antioxidant activity levels and lowest levels soluble solids
growth, which are all interconnected. In fact, positive correlations were and organic acids degradation levels, in addition to less firmness loss. In
found between these variables and vanillin content, whereas vanillin fact, the coated strawberries up to 15 days of storage included subgroups
was negatively correlated with firmness, ascorbic acid content, total with characteristics similar to those at baseline, composing the same
phenolics, antioxidant activity (FRAP and ABTS), and gallic acid con quadrant in the PCA plot, which indicates the maintenance of quality for
tent. The fact that the vanillin content showed a positive correlation a longer time. The correlation with higher h◦ values reinforces the action
with fungal growth may be related to the demonstrated ability of certain of the coatings in delaying anthocyanin synthesis, related to the senes
fungal species, such as those of the genus Aspergillus, to produce vanillin cence process, in addition to indicating lower tissue darkening; the po
through the cleavage of ferulic acid (Banerjee and Chattopadhyay, 2019; sition opposite to the vector related to BI reinforces this statement. In
Lubbers et al., 2021; Taira et al., 2018). In this case, the higher vanillin addition, the plots indicate that the control fruits exhibited an earlier
content in the control fruits corroborates the higher fungal growth correlation with events related to senescence, such as vanillin synthesis,
exhibited by them. Conversely, the fact that the coated fruits had lower tissue darkening (represented by BI), and anthocyanin synthesis – the PA
vanillin contents, taking into account the suggested hypotheses, re treatments comprised the subgroup associated with these variables
inforces the effect of the coatings in delaying the senescence processes starting on the 12th day of storage, while the control treatment already
that culminate in fruit quality loss. included the subgroup on the 6th day of storage. Although senescence
Like ascorbic acid, phenolic compounds also have a reducing effect, events, such as the increased activity of softening enzymes, cell wall
attributed to the hydroxyl group (OH), in addition to the chelating ca degradation, fungal growth, increased percentage of unfit fruits, mass
pacity of metals, such as Fe2+ and Cu+, related to fruit decay processes loss, and resveratrol synthesis, were correlated with the latest storage
(Karakaya, 2004; Min and Ebeler, 2008). In fact, positive correlations times, regardless of treatment, these correlations were weaker in the
were observed between phenolic compounds, ascorbic acid content, and coated fruits, which reinforces the effectiveness of the coatings in
antioxidant activity evaluated by the three methods (Fig. 10). Thus, the delaying these events. This statement is reinforced by the fact that the
higher antioxidant activity exhibited by the coated fruits can be attrib PA treatments starting on day 12 and the control treatments starting on
uted to the maintenance effects of these compounds through the afore day 6 formed one subgroup with the coated treatments at 18 and 21 days
mentioned mechanisms. Although there was no significant effect of the of storage, indicating that these treatments, especially the control,
coatings on the total phenolic content, they had an effect on preventing exhibited senescence events earlier than the coated treatments. In
browning (represented by the BI values) that was closely related to the addition, the fact that the PA and control groups at the end of storage
degradation of phenolic compounds, as already discussed. (days 18 and 21) formed a subgroup distinct from the coated groups at
the same storage times indicates that the senescence events were more
4.6. Fruit spoilage intense in the former, especially the control, which also formed other
distinct PA subgroups at days 18 and 21.
Although the PA fruits showed significant fungal growth later, the The fact that most of the variables studied showed significant cor
ECOSN and ECWSN strawberries maintained a lower proliferation relations among them (Fig. 10) indicates the intimate relationship be
number, especially at the end of storage, indicating the effectiveness of tween the parameters, showing that, although softening and fungal
the coatings in delaying fungal growth in strawberries. Considering that growth are the main challenges in strawberry storage, the loss of quality
the bionanocomposites do not contain any component with demon of the fruits is not associated to one or more isolated events, but to the
strated antimicrobial activity, this finding suggests that the observed combination of several variables, related directly or indirectly. Thus, the
effect on fungal spoilage is attributed to indirect mechanisms discussed initial effect of the coatings on the reduction of respiratory activity and
above, such as their O2 barrier properties that limit the activity of yeasts, metabolic rate of the fruit ends up influencing a series of other events, as
facultative anaerobes, and strictly aerobic molds (Barth et al., 2009; demonstrated throughout the work, thus proving the effectiveness of
Franco and Landgraf, 2005) and help maintain textural integrity, which coatings with ECOSN and ECWSN in extending the shelf life and main
hinders the permeation of microorganisms into the tissues. The positive taining the quality of strawberries.
correlations between fungal growth, respiratory rate, and softening
enzymes and negative correlations between fungal growth and firmness 5. Conclusions
(Fig. 10) reinforce these statements.
Lu et al. (2018) establish a classification scale for the decay rate Coating strawberries with cassava starch-based bionanocomposites
caused by strawberry molds, where 1 = no damage, 2 = mild damage reinforced with cellulosic nanofibrils from oat and wheat straw was
(<25%), 3 = moderate damage (>25% and <50%), 4 = severe damage effective in retarding the metabolism of strawberries stored at 2◦ C,
(>50% and <75%), and 5 = completely damaged (>75% and <100%). delaying and minimizing the number of senescence-related events. The
Based on this scale, the strawberries stored under the conditions of the coated strawberries performed better than those stored in sealed poly
present study showed mild to moderate damage, and the ECOSN fruits amide packages, indicating that the coatings have the potential to
reached the 21st day of storage with mild damage. replace conventional packages. In addition, the fact that the coated
In addition to being correlated with fungal growth, the percentage of strawberries performed better than the control fruits, both stored in the
unfit fruits was correlated with other events associated with senescence, same package, indicates the minimal effect exerted by the rigid poly
having shown a significant correlation with parameters such as mass propylene lid in maintaining the quality of strawberries throughout
loss, increased respiratory rate, anthocyanin synthesis, BI, firmness loss, storage, which allows us to state that the use of a second package for the
increased soluble pectin content, the activity of softening enzymes (PG coated fruits is dispensable, further reinforcing the effectiveness and
and Cx), lower antioxidant activity, lower ascorbic acid content, and potential of the coatings developed as a biodegradable alternative for
higher resveratrol content (Fig. 10). This indicates the multivariate the maintenance of the postharvest quality of strawberries. Considering
15
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Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram
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Ital. J. Food Sci. 27, 1–20. https://doi.org/10.14674/1120-1770/ijfs.v70.
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Scientia Horticulturae 309 (2023) 111668

Contents lists available at ScienceDirect

Effect of coating with co-product-based bionanocomposites on the quality

1. Introduction propensity to the attack of microorganisms, softening and, conse

2. Material and methods 2.4. Experimental design

Single 5.16 ± 292.58 ± 2.15 ± 0.54 23.43 ±

2.5. Analyses 2.5.3. Color parameters

Fig. 3. Bar graphs plots for coloration param

Fig. 4. Bar graphs and scatter lines

3.6. Fruit spoilage 3.7. PCA and Pearson correlation

CO2 0.31 -0.39*

You might also like

1 s2.0 S0304423822007828 Main PDF

Uploaded by

Copyright:

Available Formats

1 s2.0 S0304423822007828 Main PDF

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

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Copyright:

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1 s2.0 S0304423822007828 Main PDF

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Copyright:

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Scientia Horticulturae 309 (2023) 111668

Contents lists available at ScienceDirect

Effect of coating with co-product-based bionanocomposites on the quality

1. Introduction propensity to the attack of microorganisms, softening and, conse­

2. Material and methods 2.4. Experimental design

Single 5.16 ± 292.58 ± 2.15 ± 0.54 23.43 ±

2.5. Analyses 2.5.3. Color parameters

Fig. 3. Bar graphs plots for coloration param­

Fig. 4. Bar graphs and scatter lines

3.6. Fruit spoilage 3.7. PCA and Pearson correlation

CO2 0.31 -0.39*

You might also like

1. Introduction propensity to the attack of microorganisms, softening and, conse

Fig. 3. Bar graphs plots for coloration param