Industrial Crops & Products 138 (2019) 111442

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Industrial Crops & Products

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Antifungal activity of Juglans spp. and Carya sp. ethanol extracts against T
Fusarium oxysporum on tomato under greenhouse conditions
⁎
D. Jasso de Rodrígueza, , N.A. Gaytán-Sáncheza, R. Rodríguez-Garcíaa, F.D. Hernández-Castilloa,
L. Díaz-Jiménezb, J.A. Villarreal-Quintanillaa, M.L. Flores-Lópezc, D.A. Carrillo-Lomelía,
F.M. Peña-Ramosa
a
Universidad Autónoma Agraria Antonio Narro, CP 25315, Saltillo, Coahuila, Mexico
b
Cinvestav-Saltillo, Av. Industria Metalúrgica 1062, CP 25900, Ramos Arizpe, Coahuila, Mexico
c
Biocampo S.A. de C.V., Blvd. Dr. Jesús Valdés Sánchez Km. 10, Fracc. Presa de las Casas, 25350, Arteaga, Coahuila, Mexico

A R T I C LE I N FO A B S T R A C T

Keywords: Tomato fruit (Solanum lycopersicum L.) is the second most consumed vegetable worldwide. It is mainly produced
Nogalillos under greenhouse conditions; however, is highly vulnerable to the attack of pathogens. One of the most im-
Solanum lycopersicum L. portant diseases in tomato crop is the vascular wilt caused by Fusarium oxysporum, that decreases its yield up to
Fusarium wilt 60%. Recently, antimicrobial activity of the species of the Juglandaceae family has been reported, attributed to
Polyphenols
their content in polyphenols and other secondary metabolites. The aims of this work were: (1) to evaluate the
Green chemistry
antifungal activity of ethanol extracts of leaves and branches of Juglans microcarpa (JMIL and JMIB, respec-
tively), branches of Carya ovata (COB) and leaves of J. mollis (JMOL) against F. oxysporum in tomato under
greenhouse conditions; and, (2) to determine the antioxidant activity and chemical composition. The highest
values of total phenolic content (TPC) were obtained in the JMIB and JMIL and had a direct relation with the
antioxidant activity, by both 2,2 diphenyl-1-picrylhydrazil (DPPH) and ferric reducing antioxidant power
(FRAP) methods. The chemical compounds identified in the three species of nogalillos are of phenolic, terpenoid,
and fatty acids nature. The ethanol extracts of JMOL at 4000 mg L−1, JMIL at 5000 mg L−1, and COB at
5000 mg L−1, showed the greatest antifungal effect against F. oxysporum. The treatment of JMOL at
4000 mg L−1, highlighted as showed a higher growth of tomato plants and fruit quality. This is the first scientific
report on the antifungal activity of J. microcarpa, C. ovata and J. mollis against F. oxysporum in tomato crop.

1. Introduction diseases caused by fungi, are conventionally controlled using synthetic

chemicals; but, the indiscriminate use of these products has increased
Tomato fruit (Solanum lycopersicum L.) is the second most consumed the resistance of pests to most of them, and has also generated adverse
vegetable worldwide (McGovern, 2015). It is mainly produced under effects on the environment and human health (Flores-López et al.,
greenhouse conditions, which allows the control of different factors, 2016a; Yavuz and Arslan, 2013). The use of natural compounds from
such as agronomic and environmental (Erba et al., 2013). However, this plant extracts is a promising alternative for the control of phyto-
crop is affected by several diseases caused by a wide number of pa- pathogens (González et al., 2011; Jasso de Rodríguez et al., 2006), and
thogens, resulting in reduction in yield and quality of the fruits, coupled it has been reported that the use of these bioproducts is more prevalent
with large economic losses (Burketova et al., 2015; Ibrahim and Al- for application under greenhouse conditions (Paulitz and Belanger,
Ebady, 2014). One of the most important diseases is the vascular wilt 2001). Plant extracts are conformed by a matrix of bioactive and bio-
caused by Fusarium oxysporum, a soilborne pathogenic fungus that de- degradable compounds, such as the polyphenols, known by their high
creases the yield of the tomato crop by 60% (Prieto et al., 2013; antioxidant activity (Rocha-Guzmán et al., 2009; Agbenin and Marley,
Ascencio-Álvarez et al., 2008). The wilt occurs when the root is colo- 2006).
nized by the fungus, followed by the discoloration and stem necrosis, Recently, species of the Juglandaceae family have reported anti-
causing the death of the whole plant as the pathogen flows into the fungal, antibacterial, nematicide, acaricide, and insecticide activities
stems, wilting them (Bowers and Locke, 2007). Fusarium wilt and other (Garrido et al., 2014; Cruz-Vega et al., 2008; Wang et al., 2007), which

⁎
Corresponding author.
E-mail address: [email protected] (D. Jasso de Rodríguez).

https://doi.org/10.1016/j.indcrop.2019.06.005
Received 3 February 2019; Received in revised form 21 May 2019; Accepted 2 June 2019
Available online 20 June 2019
0926-6690/ © 2019 Elsevier B.V. All rights reserved.
D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

are attributed to their content in polyphenols and other secondary 2.3.2. DPPH radical scavenging activity
metabolites. In Mexico, Juglans microcarpa, Carya ovata, and J. mollis, The microplate-adapted 2,2 diphenyl-1-picrylhydrazil (DPPH) assay
commonly named as “nogalillos”, grow wild in the states of Coahuila was carried out according to Rodriguez-Jasso et al. (2014), with minor
and Nuevo León, all are considered an important source of polyphenols changes. Methanol was used as control. Each extract (5 μL) was mixed
(Salazar et al., 2008; Pérez-Calix, 2001; Senter et al., 1983). However, with 295 μL of DPPH solution (60 μmol L−1 in methanol). The solution
there is a scarcity of information about their biological activity and was mixed and kept to repose at room temperature for 30 min in the
chemical composition. For the above and continuing with the search for dark. After incubation, the absorbance was read at 517 nm. The anti-
bioactive agents of plant extracts for the control of phytopathogenic oxidant capacity was reported as percent of inhibition of DPPH, cal-
fungi of commercial importance, such as F. oxysporum, the aims of this culated with the following equation:
work were: (1) to evaluate the antifungal activity of ethanol extracts of
Abss ⎤
leaves and branches of J. microcarpa, branches of C. ovata and leaves of % DPPH inhibition = ⎡1 − x 100
⎢
⎣ ⎥
Absc ⎦ (1)
J. mollis against F. oxysporum in the crop of tomato (S. lycopersicum L.)
Saladette type, Rio Grande cv., under greenhouse conditions; and (2) to where Abss represents the absorbance value of the analyzed sample and
determine their antioxidant activity and chemical composition. Absc represents the absorbance value of the control. Experiments were
replicated in triplicate.
2. Materials and methods
2.3.3. FRAP assay
2.1. Plant collection The ferric reducing antioxidant power (FRAP) assay was determined
according to the method described by Benzie and Strain (1996), with
Branches with leaves of ten trees of each species of J. microcarpa minor modifications. The working solution of FRAP reagent was freshly
(JMI), C. ovata (CO), and J. mollis (JMO), were randomly collected in prepared before use as follows: 300 mM acetate buffer (3.1 g sodium
the states of Coahuila and Nuevo León on July 2015. They were iden- acetate trihydrate and 16 mL glacial acetic acid, pH 3.6), 10 mM TPTZ
tified in situ by the herbarium curator Dr. José Ángel Villarreal (2,4,6-tri(2 pyridyl)-s- triazine) solution in 40 mM HCl, and 20 mM
Quintanilla, and vouchers No. 097923, 084265, and 094452, were ferric chloride hexahydrate solution (10:1:1, v/v/v) were mixed, and
taken for J. microcarpa, C. ovate, and J. mollis, respectively, to deposit incubating at 37 °C for 10 min. A 10 μL aliquot of each extract was
them in the Herbarium Antonio Narro Saltillo México (ANSM) of the placed into a 96-well microplate. Then, 290 μL of FRAP reagent were
Universidad Autónoma Agraria Antonio Narro (UAAAN). The samples pipetted into each well and incubated at 37 °C for 15 min to finally read
were transported in plastic bags to the Phytochemistry Laboratory at the absorbances of the colored products (Ferrous-TPTZ complex) at
UAAAN, and immediately the leaves and branches were separated and 593 nm in a microplate reader (Synergy HT, BioTek, Winooski, VT,
dried in a stove (Mapsa, México) at 60 °C for 48 h. Then, the tissues USA). Results were expressed as microgram of Fe2+ equivalent per
were grounded using a mill (Thomas Wiley, NJ, USA) with a 2 mm sieve 100 mg of extract (μg Fe2+ 100 mg−1 extract) using a calibration curve
screen. The samples were conserved in a dried place until further use. of iron (II) sulphate solution. All the measurements were carried out in
triplicate.
2.2. Obtaining ethanol extracts
2.4. Chemical composition by gas chromatography-mass spectrometry
Ethanol extracts were obtained using a Soxhlet extractor with ab- (GC–MS)
solute ethanol as solvent, according the methodology reported by Jasso
de Rodríguez et al. (2017b). After extraction process, the solvent from The identification of the chemical composition of ethanol extracts of
the extracts was removed under low vacuum using a rotary evaporator J. microcarpa, C. ovata, and J. mollis was carried out according the
(Yamato Scientific Co., Ltd., Tokyo, Japan). The extracts were kept in a methodology described by Jasso de Rodríguez et al. (2017a). Briefly,
desiccator at 25 °C and 0% of relative humidity (RH) until their use in 2 μL of extracts previously filtered through a 0.45 μm cellulose acetate
the bioassays. membrane were injected in a GC–MS system, which consisted of an
Agilent Technologies 5850 chromatograph coupled to a mass spectro-
2.3. Phytochemical content and antioxidant activity metry MSD G3170A. Chromatographic separation was conducted using
a capillary column HP-5MS (30 m × 0.25 mm 1D × 0.25 μ), and an
Previous to the analyzes, the extracts were pre-treated according to ionization system of energy of 70 eV for detection. Helium was used as
the reported by Jasso de Rodríguez et al. (2015), with some modifica- carrier, at a constant flow of 1.1 mL min−1. The elucidation of com-
tions. Briefly, 0.02 g of each extract were mixed with 2 mL of absolute pounds was performed using the National Institute of Standards and
ethanol until complete homogenization. Afterwards, the solutions were Technology (NIST) Library.
gauged to 25 mL with distilled water.
2.5. Evaluation of extracts under greenhouse conditions
2.3.1. Total phenolic content (TPC)
The TPC was estimated by a microplate-adapted colorimetric assay 2.5.1. Greenhouse conditions
using the Folin-Ciocalteu (FC) reagent as described by Meneses et al. The study was conducted in a greenhouse at the UAAAN, in Saltillo,
(2013) with some modifications. Briefly, 5 μL of each sample was mixed Coahuila, Mexico (25°21′9.73″N latitude and 101°1′37.72″ W long-
with 60 μL of sodium carbonate solution (7.5%, w/v), and 15 μL of FC itude, 1781 masl altitude), during the cycle spring-summer of 2017.
reagent, the mixture was left to repose by 5 min. Finally, 200 μL of The greenhouse was equipped with a metallic structure covered with
distilled water were added and the solutions were mixed and left to white plastic (caliber 720) in the ceiling and lateral plates made from
repose during 5 min at 50 °C. Absorbance was measured using a mi- polycarbonate. During the experiment, the greenhouse conditions were
croplate lector (BioTek Instruments, Inc., Winooski, VT, USA) at maintained at 25 °C and 65% of RH. A high-flow drip irrigation system
700 nm. A calibration curve was prepared using a standard solution of was used in each pot; performing three diary irrigations of 600 mL of
gallic acid (GA) (0.2, 0.4, 0.6, 0.8, and 1.0 mg mL−1, R2 = 0.9919). water on each pot at three times in the day (9:00, 13:00, and 18:00 h).
Results were expressed as milligrams of GA equivalents per gram of The experiment was established under a completely randomized
extract (mg GAE 100 mg−1 extract). All experiments were performed in design with three controls: T1, absolute control (AC); T2, chemical
triplicate. control (Benomile) (CC); T3, inoculated control (IC); and six treatments

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

(ethanol extracts): T4, J. microcarpa leaves 5000 mg L−1 (JMIL 5000); plant was calculated by summing the total weight of fruits per plant,
T5, J. microcarpa leaves 4000 mg L−1 (JMIL 4000); T6, J. microcarpa obtained in the three cuts made. The number, weight, and diameter of
branches 5000 mg L−1 (JMIB 5000); T7, C. ovata branches 5000 mg L−1 the harvested fruits were counted (Pérez-Labrada et al., 2014).
(COB 5000); T8, J. mollis leaves 5000 mg L−1 (JMOL 5000), and T9, J.
mollis leaves 4000 mg L−1 (JMOL 4000). The parts of species and the
2.8. Fruit quality parameters
concentration of the extract used in each treatment, were selected ac-
cording to their antifungal activity in vitro against F. oxysporum, pre-
Fruit firmness, pH and soluble solids (TSS), and antioxidants were
viously reported by Jasso de Rodríguez et al. (2016).
measured in tomatoes harvested at the end of the crop.
2.5.2. Preparation of stock solutions of extracts and fungal inoculum of F.
oxysporum 2.8.1. Fruit firmness
Stock solutions of each extract of J. microcarpa, C. ovata, and J. Firmness was measured using five tomatoes per treatment, which
mollis were prepared at 10,000 mg L−1 by mixing 40 g of extract with were cut from the first cluster (Pérez-Labrada et al., 2014). Briefly,
10% of absolute ethanol and completed to volume of 2000 mL with using a penetrometer (QA supplies, Norfolk, VA, USA) with an 8 mm
distilled water, then sonicated (Bransonic Ultrasonic Cleaner 5510, lace, the tomato bark was perforated until reaching the pulp, holding
Danbury, CT, USA) for 30 min. Immediately, they were stored in an firmly the penetrometer. Results were expressed in kilograms per
amber flask at room temperature until further use. square centimeter (kg cm−2).
The F. oxysporum was obtained from the UAAAN collection. The
strain was cultured on potato dextrose agar (PDA) medium at 25 °C for
2.8.2. pH and total soluble solids (TSS)
12 d. Subsequently, the spore suspension at concentration of 6.2 × 107
Before the analyzes, tomato samples (50 g) of each treatment were
spores mL−1 was obtained as described by Flores-López et al. (2016b),
ground in a blender and filter using filter paper Whatman no. 1 under
with some modifications.
vacuum. The pH was measured by direct immersion of the electrode
with a potentiometer (HANNA Instruments Inc., Romania), previously
2.5.3. Inoculation and treatments application
calibrated. The TSS were measured with a refractometer (ATAGO Co.
Two months seedlings of determinate cycle with five to six true
Ltd., Japan) according to the 932.12 Association of Official Analytical
leaves of tomato (S. lycopersicum L.) Saladette type, Rio Grande cv.,
Chemists (AOAC) method (AOAC, 1997). The results of TSS in the fruits
were used. The seedlings were inoculated by the method of root im-
were expressed as percentage (%). All the experiments were conducted
mersion in the F. oxysporum spore solution (Di Pietro and Roncero,
using three samples per treatment.
1998). Briefly, cuts were made in the root ball of each seedling, with
sterile scissors. Subsequently, the roots were immersed during 20 min in
the spore solution. Then, transplant was carried out in plastic pots of 2.8.3. Antioxidants
12 L, using as substrate a mixture of Peat moss, perlite, and zeolite 2.8.3.1. Lycopene. In order to determine the lycopene content, a
(5:5:1). The pots were placed with a distance of 50 cm between each sample of 0.25 g ground tomato was mixed with 15 mL of a
plant, and 75 cm between rows. The pots were distributed under a hexane:acetone (v/v) solution. The mixture was stirred for 30 min,
completely randomized design, with nine treatments and ten repeti- and distilled water was added to separate the polar compounds of the
tions, with a total of 90 plants. Each experimental unit consisted of a extraction. Finally, the mixture was filtered through a 0.45 μm cellulose
tomato plant. acetate membrane. A volume of 5 μL of sample was injected in a high-
In the transplant, 100 mL of each treatment were applied directly to performance liquid chromatography (HPLC). The system consisted in
the root system; later, 100, 300, and 300 mL were applied at 10, 20, and an Agilent 1200 HPLC system with a quaternary bomb, auto sampler,
40 d after transplant (DAT), respectively. Tomato plants were main- and a Zorbax Eclipse XDB-C18 column (150 × 4.6 mm 5 μm). The
tained during 125 d under greenhouse conditions, period in which the detection was made with visible light at 472 nm, the mobile phase was
parameters of severity and incidence, phenological and production, and isocratic consisting of 30% of ethanol and 70% of methanol (v/v), at a
quality of the fruits were evaluated. flow rate of 1 mL min−1 (Arias et al., 2000). The results were expressed
in milligrams of lycopene per 100 gram of tomato (mg lycopene 100
2.6. Incidence and severity g−1 tomato).

Incidence was determined by counting the number of diseased

2.8.3.2. Vitamin C. The Vitamin C content was estimated according to
plants in relation to the total number of the plants per treatment. The
the method described by Gutierrez et al. (2007). Samples of tomato
percentage of incidence was calculated as follows:
(6 g) were mixed with 25 mL of phosphoric acid solution (0.05 N) and
Diseased plants stirred during 30 min. Afterwards, the mixture was centrifuged at
% Incidence= x 100
Total plants (2) 3000 rpm for 10 min, and filtered with a 0.22 μm membrane filter.
The solution was maintained at 4 °C, and then analyzed by an Agilent
Severity was determined by visual evaluation, and values were
1200 HPLC using a C18 column under an isocratic mobile phase
given according to the scale proposed by Kurabachew et al. (2013),
NaH2PO4 1% (v/v), pH = 2.7 at flow rate of 0.9 mL min−1. The
where values from 0 to 5 are related to the symptoms of leaf necrosis
wavelength used to detect vitamin C was 265 nm. The results were
wilt: 0 = no wilt symptoms, 1 = one leaf wilted, 2 = two leaves wilted,
expressed in milligrams of vitamin C per 100 g of tomato (mg vit C 100
3 = three leaves wilted, 4 = wilting of all leaves without tip, and 5 =
g−1 tomato).
total wilting of the plant (dead plant).

2.7. Growth and yields 2.9. Statistical analysis

To determine the effect on vigor of tomato plants of the treatments Data analyses were performed using analysis of variance (ANOVA).
the following paraments were measured: the diameter (mm) and length Fisher’s Least Significance Difference (LSD) multiple comparison test
(cm) of the stem at 97 DAT. The number of leaves and flowers per plant was performed to detect significant differences (p < 0.05) between
were weekly counted; the dry biomass (g), root lenght (cm), and root treatments with SAS-PC software (v.9) for Windows. For severity, the
weight (g) were determined at 125 DAT. The production of fruit per data were analyzed by Kruskal-Wallis test (p < 0.05)

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

Table 1 extracts of leaves of J. microcarpa, which its antioxidant activity is well

Total phenolic content and antioxidant activity of ethanol extracts of nogalillos. known (Berton et al., 1998) (Table 2). In this extract was also presented
Extract Antioxidant activity the benzeneethanamine, 2-fluoro-β,3-dihydroxy-N-methyl- (phenolic
amine, nature), and phytol (diterpene nature), which possess anti-
−1
TPC (mg GAE 100 mg DPPH (%) FRAP (μg Fe2+100 mg−1 microbial and antibacterial activities, respectively (Muthuraman et al.,
extract) extract) 2012; Inoue et al., 2005). In relation to the extract of the branches of J.
JMIL 28.7 ± 0.2b 89.6 ± 1.1a 69.4 ± 3.3a microcarpa, juglone (a naphthalene derivative) was identified in low
JMIB 32.1 ± 0.3a 77.7 ± 7.0b 43.7 ± 2.6b concentration (1.0%), this agrees with the results obtained by Pereira
COB 24.8 ± 0.7c 64.5 ± 3.6c 31.0 ± 0.8c et al. (2007). Juglone has been reported by its antifungal and anti-
JMOL 13.6 ± 0.3d 74.4 ± 3.9bc 36.1 ± 1.3d oxidant activities (Chobot and Hadacek, 2009; Clark et al., 1990); also,
hexadecanoic acid, ethylester, and ethyl linoleate were detected, which
JMIL: Juglans microcarpa leaves; JMIB: J. microcarpa branches; COB: Carya
ovata branches; JMOL: J. mollis leaves.
have exhibited nematicide and antifungal activities (Rajeswari et al.,
Values in the same column followed by different letters are statistically different 2012; Agoramoorthy et al., 2007). There are no reports about chemical
(p < 0.05). composition and biological activity of J. microcarpa extracts; but, ac-
cording with the results found here, it can be expected the potential
3. Results and discussion antifungal, antimicrobial, nematicide, and antioxidant activities.

3.1. Phenolic content and antioxidant activity 3.2.2. Carya ovata

The chemical profile of the ethanol extracts of C. ovata showed five
The ANOVA showed significant differences (p < 0.05) in the TPC compounds (Table 3). It is important to observe the presence of juglone,
of the ethanol extracts of nogalillos under study, being in the following a typical phenolic compound of the Juglans spp. with antioxidant ac-
order: JMIB > JMIL > COB > JMOL (Table 1). The results evidenced tivity (Wianowska et al., 2016; Pereira et al., 2007). This compound is
variations even among the same species, when evaluating different found in low concentrations in dry leaves, but in this study was detected
parts of the plant (leaves and branches). in dry branches. The major compounds in this extract are: 9,12-octa-
Recent works have reported the positive relation between the TPC decadienoic acid ethyl ester (31.9%), ethyloleate (11.3%), and hex-
and antioxidant activity (Flores-López et al., 2016b; Cerqueira et al., adecanoic acid ethylester (10.3%), all of them of fatty ester nature,
2010). This behavior was also observed in this work, as the J. micro- which have antibacterial, antifungal, antioxidant, and nematicide ac-
carpa extracts showed the highest TPC values (p < 0.05) and conse- tivities (Rajeswari et al., 2012; Agoramoorthy et al., 2007). The above
quently, the highest (p < 0.05) antioxidant activity detected by two suggests that from this extract it may be feasible to obtain antimicrobial
methods of analysis (DPPH and FRAP). Good correlation was found products. This is the first report on the chemical composition of C.
between both antioxidant methods in agreement with the obtained in ovata.
literature (López et al., 2013).
To date, no reports have been published on TPC and antioxidant 3.2.3. Juglans mollis
activity for J. microcarpa and C. ovata; however, there is extensive in- The ethanol extracts of leaves of J. mollis presented ten compounds
formation on J. regia L. Oliveira et al. (2008) reported TPC values in the (Table 4), four of them also identified in J. microcarpa (three in leaves,
range of 3.3–7.5 mg GAE 100 mg−1 for aqueous extract of green husks and one in branches, Table 2). The hexanedioic acid dioctyl ester, a
of five cultivars of J. regia, which are lower than those obtained in this fatty acid ester, was the major compound with 16.5%, this has shown
study. Salazar et al. (2008) conducted a phytochemical study of several antibacterial and antifungal activities (Rajeswari et al., 2012;
species, including extracts of J. mollis leaves. These presented TPC va- Agoramoorthy et al., 2007). Another fatty acid ester, the hexadecenoic
lues higher (22.3 mg catechol 100 mg-1 extract) than those found here acid, ethyl ester (11.2%) was detected, which possesses antioxidant
(13.6 ± 0.3 mg GAE 100 mg-1 extract), though the authors reported capacity (Rajeswari et al., 2012). Also, antifungal and antimicrobial
similar antioxidant activity (77.6%) that those obtained in this study for compounds were detected in this extract, but in minor quantities, such
J. mollis leaves (74.4 ± 3.9%) (Table 1). The differences in TPC can be as methyl (Z)-5,11,14,17-eicosatetraenoate (7.6%), and 1-methoxy-3-
attributed to the sampling intervals existing between both studies (2-hydroxyethyl)nonane (3.2%) (Rajeswari et al., 2012; Hashem,
(approximately, 12 years), factor that changes the environmental con- 2011). Inbaraj and Chignell (2004) reported the presence of an im-
ditions in which the plants were developed, and thus the content of portant quantity of non-polar compounds in the bark of J. mollis with
phenolic compounds (Silva et al., 2012). In addition, the solvents used antibacterial activity. In general, the compounds identified in this ex-
in obtaining extracts (methanol and ethanol), can influence in the TPC, tract have been previously reported with antifungal, antibacterial, and
but in a low proportion (Rodrigues et al., 2018). nematicide activities, which stands out its bioactive potential.

3.3. Incidence and severity

3.2. Chemical composition by GC-MS
The ANOVA for incidence and severity indicated differences
Chemical composition results obtained for nogalillos ethanol ex-
(p < 0.05) between treatments (Table 5). All treatments provided
tracts are shown in Tables 2–4. Most of the compounds detected by GC-
protection to the plant against the attack of F. oxysporum, highlighting
MS, are from the nitrogenous and oxygenated hydrocarbons groups.
the treatments of JMIL 5000 and JMOL 5000 (both with 37.5% of in-
cidence). These showed a minor incidence (%) when compared with the
3.2.1. Juglans microcarpa other treatments with extracts. It was expected that the inoculated
A total of 19 compounds were identified in the ethanol extracts of J. control (IC) showed the higher (p < 0.05) levels of incidence (100%),
microcarpa; being interesting the detection of different compounds in as the plant was directly exposed to the pathogen without protection;
one and another tissue: eight in leaves and eleven in branches at dif- however, also the plants treated with chemical fungicide (CC) presented
ferent concentrations (Table 2). This has been observed in other plants, 100% of incidence. This can be explained by the fact that the indis-
such as Heteropterys tomentosa, which contains catechin, rutin, and criminate use of chemical fungicides has caused pest resistance (Flores-
chlorogenic acid in the leaves; whereas, taxifolin is only detected in the López et al., 2016a).
branches (Paula-Freire et al., 2013). In regards to severity, the six treatments and the absolute control
Vitamin E acetate was the major compound (13.6%) in the ethanol were not statistical different (p > 0.05), and presented lower

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

Table 2
Chemical compounds identified in the ethanol extracts of leaves and branches of Juglans microcarpa.
Compound Area (%) Biological activity Reference

Leaves Branches

Propanamide, 2-hydroxy- 2.4 – NR –

2-Formyl histamine 1.7 – Antimicrobial Muthuraman, et al., 2012
Juglone – 1.0 Antimicrobial, antioxidant Clark et al., 1990; Chobot and Hadacek, 2009
Hydrastininic acid 1.3 – Antibacterial Gong et al., 2015
Viridiflorol – 1.6 Anti-inflammatory Manzano-Santana et al., 2009
Spathulenol – 0.5 Antioxidant Ziaei et al., 2011; Martins et al., 2010
3,6,9,12-Tetraoxatetradecan-1-ol, 14-[4-(1,1,3,3-tetramethylbutyl) – 0.7 NR —
phenoxy]-
14-Octadecenal – 0.5 Antioxidant Liu et al., 2007
Benzeneethanamine, 2-fluoro-β,3-dihydroxy-N-methyl- 2.0 – Antimicrobial Muthuraman et al., 2012
n-Hexadecanoic acid – 1.1 Nematicide Kumar et al., 2010
Hexadecanoic acid, ethyl ester – 3.0 Antioxiodant, nematicide Rajeswari et al., 2012
13-Heptadecyn-1-ol – 1.2 Antiviral Ogunlesi et al., 2009
Benzeneethanamine, 2,5-difluoro-β,3,4-trihydroxy-N-methyl- 1.8 – Antioxidant –
Phytol 4.7 – Antibacterial Inoue et al., 2005
Ethyl linoleate – 4.3 Antibacterial, antifungal Agoramoorthy et al., 2007; Rajeswari et al.,
2012
2,2,4-Trimethyl-3-(3,8,12,16-tetramethyl-heptadeca-3,7,11,15-tetraenyl)- – 4.5 NR –
cyclohexanol
Stigmastan-3-ol, 5-chloro-, acetate, (3β,5α)- – 2.7 NR –
Phenol, 2,2'-methylenebis[6-(1,1-dimethylethyl)-4-ethyl- 3.3 – NR –
Vitamin E acetate 13.6 – Antioxidant Berton et al., 1998

NR: Not reported.

(p < 0.05) severity index than the inoculated and chemical controls. tannins.
There are no reports in literature on studies of antifungal activity of the Based on the above, the reduction of severity and incidence rates in
species under study on tomato crop. However, evaluations of the an- tomato plants treated with the extracts of nogalillos species under
tifungal effects of other species of the Juglandaceae family have been study, may be promoted by the matrix of chemical compounds present
published. Osorio et al. (2010) evaluated the antifungal activity in vitro in the extracts identified by GC-MS (Tables 2 –4). These compounds are
of polyphenolic extract of Pecan nutshell (C. iIllinoensis) against the of different nature: phenolic, diterpene, polyol, and fatty acid, which
phytopathogenic fungi Phytium sp, Colletotrichum truncatum, C. coc- have been reported for their antifungal, antimicrobial, and nematicidal
codes, Alternaria alternata, F. verticilloides, F. solani, F. sambucinum, and activities (Muthuraman et al., 2012; Rajeswari et al., 2012; Chobot and
Rhizoctonia solani, and ten strains of F. oxysporum. The polyphenolic Hadacek, 2009 Agoramoorthy et al., 2007; Inoue et al., 2005; Clark
extract of C. iIllinoensis showed a high activity to inhibit mycelial et al., 1990). Further research is needed to elucidate the antifungal and
growth in these fungi, as well as in 50% of strains of F. oxysporum; other potential bioactivities of the compounds present in the extracts of
which evidenced the antifungal activity against a large number of the species of nogalillos investigated in this work.
phytopathogenic fungi. The authors cited that the antifungal activity
can be based on the capacity of the poly- and monomeric phenols to
form complexes with polysaccharides and proteins of external layers of 3.4. Growth, yield, and quality of fruit
the fungal cells that destabilize the functions of the cell walls and
membranes, causing the death of microorganisms. Wianowska et al. The ANOVA for stem length showed significant variation
(2016) reported antifungal effect of walnut green husks extracts of five (p < 0.05), as shown in Fig. 1. A significant increase of 19% in stem
cultivars of J. regia, as well as of juglone, against A. alternata, R. solani, length was observed with the application of the JMOL 4000 treatment,
B. cinerea, F. culmorum, and Phytophtora infenstans. The authors asso- followed by JMIL 5000, and JMIB 5000 with increases of 7.1% and
ciated such activity to the presence of other phenolic compounds 7.7%, respectively, with respect to the plants inoculated with F. oxy-
identified in the extracts, in addition to the juglone. sporum (IC). This result evidenced the ability of these extracts to control
Upadhyay et al. (2010) evaluated the antifungal activity and de- the Fusarium wilt, as the plants continued their growth during the study.
termined the phytochemical composition of seven extracts of stem bark It should be noted that the inhibition of the longitudinal growth of the
of J. regia, obtained with different solvents (petroleum ether, benzene, stem is a characteristic symptom of F. oxysporum f. sp. lycopersici
chloroform, acetone, methanol, ethanol, and water), against Aspergillus (Carrillo-Fasio et al., 2003; Cai et al., 2003). Meanwhile, the mean
niger, A. alternata, Trichoderma virens, and F. solani. The methanol ex- values of stem diameter of the plants observed with all the treatments
tract had the highest antifungal activity, which was attributed to were similar to those for the inoculated control (Fig. 2). There is no
identified phytocompounds: alkaloids, carbohydrates, flavonoids, and scientific works about the evaluation of these parameters with noga-
lillos extracts; however, Nefzi et al. (2016) used aqueous extracts of

Table 3
Chemical compounds identified in the ethanol extract of the branches of Carya ovata.
Compound Area (%) Biological activity Reference

Juglone 2.8 Antibacterial, antioxidant Clark et al., 1990; Chobot and Hadacek, 2009
2-Trifluoroacetoxydodecane 4.2 Antimicrobial Rahbar et al., 2012
Hexadecanoicacid, ethylester 10.3 Antioxidant, nematicide Rajeswari et al., 2012
9,12-Octadecadienoic acid, ethylester 31.9 Antibacterial, antifungal Agoramoorthy et al., 2007; Rajeswari et al., 2012
Ethyl oleate 11.3 Antibacterial, antifungal Agoramoorthy et al., 2007; Rajeswari et al., 2012

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

Table 4
Chemical compounds identified in the ethanol extract of the leaves of Juglans mollis.
Compound Area(%) Biological activity Reference

Propanamide, 2-hydroxy- 2.2 NR –

2-Nonanol 1.6 NR –
Hydrastininic acid 1.0 Antitussive Gong et al., 2015
1-Methoxy-3-(2-hydroxyethyl)nonane 3.2 Antifungal Hashem, 2011
2,4-Bis(hydroxilamino)-5-nitropyrimidine 2.7 NR –
Hexadecanoic acid, ethyl ester 11.2 Antioxidant Rajeswari et al., 2012
Pterin-6-carboxylic acid 4.0 NR –
Methyl (Z)-5,11,14,17-eicosatetraenoate 7.6 Antibacterial, antifungal Agoramoorthy et al., 2007; Rajeswari et al., 2012
Benzeneethanamine, 2,5-difluoro-β,3,4-trihydroxy-N-methyl- 4.5 NR –
Hexanedioic acid dioctyl ester 16.5 Antibacterial, antifungal Agoramoorthy et al., 2007; Rajeswari et al., 2012

NR: Not reported.

Table 5 from Fusarium wilt, and also induced the weight gain of the different
Severity and incidence caused by Fusarium oxysporum in tomato plants. parts of the plant.
Treatment (mg L−1) 1
Incidence (%) 2
Severity (grade) Regarding the root length, the absolute and chemical controls
showed the longest length, the increase with respect to IC was 17.5%
b
AC 37.5 0.4a and 19.2%, respectively. However, with the exception of JMIL 5000,
CC 100.0a 1.3bc the other five extracts were statistically similar to the inoculated
IC 100.0a 2.4c
JMIL 5000 37.5b 0.4a
treatment for this variable. Schinzoumka et al. (2016) reported the
JMIL 4000 62.5ab 0.9ab increase in the weight of aerial parts and roots in tomato plants cv. Rio
JMIB 5000 87.5a 0.9ab Grande when applied extracts of Acacia albida and Crotalaria retusa
COB 5000 62.5ab 0.6ab obtained with different solvents.
JMOL 5000 37.5b 0.5a
The number of leaves, flowers, and fruits accumulated in the cycle,
JMOL 4000 75.0ab 0.8ab
and fruit yield per plant is presented in Table 7. The application of
AC: absolute control; CC: chemical control (Benomile); IC: inoculated control; JMOL 4000 allowed to obtain the highest average number of leaves
JMIL: Juglans microcarpa leaves; JMIB: J. microcarpa branches; COB: Carya (48.8) and flowers (59.3); whereas, the IC treatment had the lowest
ovata branches; JMOL: J. mollis leaves. number of leaves and flowers (37.0 and 34.0, respectively). The other
Values in the same column followed by different letters are statistically dif- treatments were statistically similar in both variables. The JMIL 5000
ferent. treatment had the highest number of fruits (41), and the JMOL 5000
1
LSD (p < 0.05). treatment had the lowest one (26.6). The other seven treatments were
2
Kruskal-Wallis (p < 0.05).
not statistically different. In terms of yield, the highest value was for
COB 5000 (2.1 kg per plant), but was not statistically different with the
Lycium arabicum against F. oxysporum in tomato plant, achieving the other treatments. The lowest yields (1.6 and 1.5 kg per plant for JMIL
decrease of the disease and enhancing the growth of the stem length 4000 and JMOL 5000, respectively) correspond to those plants with
and diameter. lower number of fruits (28.5 and 26.6, respectively). However, these
A significant increase (p < 0.05) was observed in the weight of results are superior to those reported by Rodríguez and Montilla (2002).
leaves, stem, and root with the JMOL 4000 treatment with respect to The authors found yields in the range of 0.52–1.4 kg per tomato plant,
inoculated treatment (Table 6), being the weight increases of 68.1%, with the weekly application of an extract of Citrus paradisi in soil, roots,
54.2%, and 71.1%, respectively. The other treatments based on extracts and foliage, to reduce Fusarium wilt.
had lower weight in these variables when compared with those ob- The results of nogalillos ethanol extracts found in this work, suggest
tained with JMOL 4000, but higher in weight of leaves and root, and their potential protective effect against the attack of F. oxysporum,
similar in stem weight with respect to the IC treatment. Corpas-Hervias benefiting the development of the plant as well as the fruit and yield of
et al. (2006) cited that F. oxysporum can reduce the root biomass by up tomato crop.
to 75%. The JMOL 4000 extract managed to protect the tomato plants The quality paraments of polar and equatorial diameter, firmness,

Fig. 1. Main stem growth of tomato Saladette type, Rio Grande cv. treated with ethanol extracts of nogalillos, at 97 DAT. Different letters indicate significant
differences (p < 0.05).

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

Fig. 2. Growth of stem diameter (mm) in tomato Saladette type, Rio Grande cv. treated with ethanol extracts of nogalillos, at 97 DAT. Different letters indicate
significant differences (p < 0.05).

Table 6 Table 8
Mean comparison of growth rate parameters of tomato plants: dry weight (g) of Effect of ethanol extracts on fruit quality parameters of tomato plants.
leaves, branches and roots, and root length (cm).
Treatments Polar Equatorial Firmness (kg TSS (%) pH
Treatments (mg L−1) Dry weight (g) Root length (cm) (mg L−1) diameter diameter (mm) cm−2)
(mm)
Leaves Branches Root
AC 56.4abc 47.7a 3.1c 3.8c 4.2cd
AC 54.1bc
29.1 ab
5.6ab 69.5ab CC 55.7abc 47.3ab 4.3bc 4.6ab 4.5a
CC 53.0bc 23.4bc 5.6ab 70.5a IC 54.5bc 45.5b 6.2abc 4.9a 4.4ab
IC 47.6c 21.4bc 3.8b 59.1bcd JMIL 5000 53.6c 45.2bc 4.1bc 5.0a 4.0d
JMIL 5000 65.9ab 26.5abc 4.3b 55.9cd JMIL 4000 55.3abc 46.9ab 3.9bc 4.9a 4.1cd
JMIL 4000 50.0c 19.5c 4.0b 49.9d JMIB 5000 54.7abc 44.7c 5.5abc 4.6ab 4.1cd
JMIB 5000 59.6bc 23.1bc 5.0ab 64.7abc COB 5000 54.8abc 46.5abc 6.7ab 4.3bc 4.1cd
COB 5000 58.1bc 22.4bc 5.1ab 61.8abc JMOL 5000 57.4ab 46.8abc 8.4a 4.5ab 4.0cd
JMOL 5000 59.1bc 23.8bc 4.6b 57.0cd JMOL 4000 57.6a 47.3ab 5.8abc 4.9a 4.2bc
JMOL 4000 80.9a 33.0a 6.5a 60.7abc CV (%) 5.2 4.5 49.2 9.1 4.1
CV (%) 26.1 32.4 36.6 17.3
AC: absolute control; CC: chemical control (Benomile); IC: inoculated control;
AC: absolute control; CC: chemical control (Benomile); IC: inoculated control; JMIL: Juglans microcarpa leaves; JMIB: J. microcarpa branches; COB: Carya
JMIL: Juglans microcarpa leaves; JMIB: J. microcarpa branches; COB: Carya ovata branches; JMOL: J. mollis leaves.
ovata branches; JMOL: J. mollis leaves. Values in the same column followed by different letters are statistically different
Values in the same column followed by different letters are statistically different (p < 0.05).
(p < 0.05).
retards vegetative growth and improves the quality of the fruits.
Table 7 In relation to pH, the results ranging of 4.0–4.5 (Table 8), values in
Effect of plant extracts on production parameters of tomato plants. agreement with those reported by Cantwell (2006) for tomato fruits. It
Treatments (mg L−1) Leaves Flowers Fruits Yield is observed that the pH values decreased (p < 0.05) in all the treat-
(Number per plant) (kg per plant) ments based on extracts with respect to the chemical and inoculated
control. The highest values (p < 0.05) were detected for CC and IC,
AC 47.3ab 32.6abc 39.4c 1.9ab
that can be related with the maturation process of the fruit accelerated
CC 42.0ab 38.4ab 53.1ab 2.1ab
IC 37.0b 34.0abc 37.8c 1.8ab by the attack of F. oxysporum, as these had higher incidence (Table 5)
JMIL 5000 40.8ab 41.0a 48.1abc 2.0ab (Athmaselvi et al., 2013).
JMIL 4000 41.0ab 28.5bc 39.8bc 1.6b Otherwise, values of TSS in tomato fruits for all the treatments
JMIB 5000 47.8ab 32.0abc 49.4abc 1.7ab ranged between 3.8–5.0%, which is in agreement with the values re-
COB 5000 46.1ab 36.6ab 48.1abc 2.1a
JMOL 5000 42.4ab 26.6c 47.4abc 1.5b
ported by Zapata et al. (2008). No significant differences (p > 0.05)
JMOL 4000 48.8a 33.8abc 59.3a 1.9ab were detected in the TSS between treatments; but, the lowest value in
CV (%) 26.7 29.6 28.7 32.3 absolute control is observed (3.8%). Bhattarai and Gautam (2006) in-
dicated that the increase of TSS in the maturation phase is due to the
AC: absolute control; CC: chemical control (Benomile); IC: inoculated control; increase of the sugar concentration in fruits when the loss of water
JMIL: Juglans microcarpa leaves; JMIB: J. microcarpa branches; COB: Carya
occurs. In the present study, the lack of water in the plant can be at-
ovata branches; JMOL: J. mollis leaves.
tributed to the wilting of the plant caused by F. oxysporum.
Values in the same column followed by different letters are statistically different
(p < 0.05).
Regarding fruit firmness, the treatments with the extracts presented
a range of 3.9 to 8.4 kg cm−2 (Table 8). The highest value was for JMOL
TSS, and pH are presented in Table 8. For polar diameter, the treat- 5000 (8.4 kg cm−2), but it was not significantly different from the re-
ments JMOL 5000 and JMOL 4000 presented the largest diameter (57.4 sults for JMOL 4000, COB 5000, JMIB 5000, and IC treatments. The
and 57.6 mm, respectively), whilst smaller diameter was for JMIL 5000; lowest value was for the absolute control (3.1 kg cm−2). The reduction
even though these differences were not statistically significant. This in the firmness is consequence of enzymatic degradation of pectin and
increase in size is similar to that reported by Ramírez et al. (2016), who starch of the fruit cell wall, being these actions closely linked to the fruit
demonstrated an increase in the size of tomato fruits with the appli- ripening progress (Ali et al., 2010).
cation of bioregulators such as prohexadione of calcium (P-Ca), that Tomato fruit is a natural source of vitamin C and lycopene; and their

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

Fig. 3. Effect of ethanol extracts of nogalillos on the lycopene content (mg 100 g−1 tomato) of fruits of tomato Saladette type, Rio Grande cv. Different letters indicate
significant differences (p < 0.05).

Fig. 4. Effect of ethanol extracts of nogalillos on the vitamin C content (mg 100 g−1 tomato) of fruits of tomato Saladette type, Rio Grande cv. Same letters did not
differ by LSD’s test (p > 0.05).

levels are reduced during maturation, being used as an indicator of environment and human health. The results obtained are promising, as
postharvest quality (Souza et al., 2015; Athmaselvi et al., 2013). The the antifungal activity of the extracts of three species of wild nogalillos
lycopene contents in the fruits were in the range of 35.5 to 82.9 mg 100 against F. oxysporum was proved in tomato plants. In addition, the
g−1 tomato, which presented significant difference between treatments antioxidant activity and the chemical composition of the evaluated
(Fig. 3). Loganathan et al. (2014), reported that the application of Ba- extracts were identified. These findings may be the basis for an appli-
cillus subtillus, in addition to controlling F. oxysporum, promoted high cation project and provide a value-added to these species that have no
lycopene content (7.6 mg 100 g−1 tomato). The treatments based on commercial-economic use.
nogalillos extracts showed higher (p < 0.05) contents of lycopene. The
vitamin C ranging from 9.5 to 13.3 mg vit C 100 g-1 tomato, showing
not statistical differences between treatments (Fig. 4). Ramírez et al. 4. Conclusions
(2016) reported vitamin C content in the range of 14.0 to 20.0 mg vit C
100 g-1 tomato, with the application of bioregulators in tomato. These The ethanol extracts of J. mollis leaves at 4000 mg L−1, J. microcarpa
results are higher than those reported in the present study. Tokunaga leaves at 5000 mg L−1, and C. ovata branches at 5000 mg L−1, showed
et al. (2005) reported that antioxidants are increased under conditions the best antifungal effect against F. oxysporum. On the other hand, the
of biotic stress, as they participate in the inactivation of reactive oxygen extract of J. mollis leaves at 4000 mg L−1 exhibited a greater effect on
species. Based on this fact, it can be suggested that the forced invasion the growth of the tomato plants and allowed fruits with better quality.
of F. oxyposporum conducted on tomato plants caused stress, promoting Ethanol extracts of nogalillos were characterized by the presence of
the lycopene content, more accentuated in the IC and CC treatments. polyphenolic compounds, such as terpenoids and fatty acids, which
The results of this work highlight the relevance of the new research have been reported for their antibacterial and antifungal activities.
stage on nogalillos, which pretends the in vivo application of bioactive Further studies on the isolation, characterization, and antifungal
plant extracts from the semi-arid zones of Mexico as main focus. The activity of compounds presented in the nogalillos extracts are required
development of green chemistry for application in agriculture is an to determine which are responsible for such bioactivity.
alternative to reduce the use of synthetic fungicides, which affect the This is the first scientific report of the antifungal activity of J. mi-
crocarpa, C. ovata, and J. mollis in tomato crop. Therefore, it is necessary

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D. Jasso de Rodríguez, et al. Industrial Crops & Products 138 (2019) 111442

to continue with the research in order to determine periods of appli- Phytother. Res. 4, 11–14. https://doi.org/10.1002/ptr.2650040104.
cation during the development of the crop, and additional effects re- Corpas-Hervias, C., Melero-Vara, J.M., Molinero-Ruiz, M.L., Zurera-Muñoz, C., Basallote-
Ureba, M.J., 2006. Characterization of isolates of Fusarium spp. obtained from as-
lated from the application of such products (e.g. inductions of systemic paragus in Spain. Plant Dis. 90, 1441–1451. https://doi.org/10.1094/PD-90-1441.
resistance, growth promoting effect, increase of bioactive compounds, Cruz-Vega, D.E., Verde, S.M.J., Salinas, G.N., Rosales, H.B., Estrada, G.I., Mendez, A.P.,
among others). Also, it is important to elucidate the mechanisms of Carranza, R.P., González, G.M.T., Castro, G.J., 2008. Antimycobacterial activity of
Juglans regia, Juglans mollis, Carya illinoensis and Bocconia frutescens. Phytother. Res.
action of the extracts in the control of F. oxysporum, as well as the re- 22, 557–559. https://doi.org/10.1002/ptr.2343.
sponse of the tomato growth and quality variables to the application of Di Pietro, A., Roncero, M.I.G., 1998. Cloning, expression, and role in pathogenicity of pg1
the extracts. encoding the major extracellular endopoly galacturonase of the vascular wilt pa-
thogen Fusarium oxysporum. Mol. Plant Microbe Interact. 11, 91–98. https://doi.
org/10.1094/MPMI.1998.11.2.91.
Acknowledgements Erba, D., Casiraghi, M.C., Ribas-Agustí, A., Cáceres, R., Marfà, O., Castellari, M., 2013.
Nutritional value of tomatoes (Solanum lycopersicum L.) grown in greenhouse by
different agronomic techniques. J. Food Anal. 31, 245–251. https://doi.org/10.1016/
Author N.A. Gaytán-Sánchez thanks Mexican Science and
j.jfca.2013.05.014.
Technology Council (CONACYT, Mexico) for MSc fellowship support. Flores-López, M.L., Cerqueira, M.A., Jasso de Rodríguez, D., Vicente, A.A., 2016a.
Authors would like to thank to María Guadalupe Moreno Esquivel, Perspectives on utilization of edible coatings and nano-laminate coatings for exten-
Edith E. Chaires Colunga, Olga L. Solís Hernández, and M. Leticia sion of postharvest storage of fruits and vegetables. Food Eng. Rev. 8, 292–305.
https://doi.org/10.1007/s12393-015-9135-x.
Rodríguez González of the Phytochemistry Laboratory from Flores-López, M.L., Romaní, A., Cerqueira, M.A., Rodríguez-García, R., Jasso de
Universidad Autónoma Agraria Antonio Narro, for their assistance in Rodríguez, D., Vicente, A.A., 2016b. Compositional features and bioactive properties
obtaining extracts and chemical composition. of whole fraction from Aloe vera processing. Ind. Crops Prod. 91, 179–185. https://
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