Preharvest Application of Methyl Jasmonate as an Elicitor Improves

Sep 29, 2017 - The effects of methyl jasmonate (MeJa) treatment as an elicitor of artichoke plants [Cynara cardunculus var. scolymus (L.) Fiori] on th...
42 downloads 12 Views 1MB Size
Download PDF
Article pubs.acs.org/JAFC

Cite This: J. Agric. Food Chem. 2017, 65, 9247-9254

Preharvest Application of Methyl Jasmonate as an Elicitor Improves the Yield and Phenolic Content of Artichoke Alejandra Martínez-Esplá,† Daniel Valero,† Domingo Martínez-Romero,† Salvador Castillo,† María José Giménez,† Maria Emma García-Pastor,† María Serrano,‡ and Pedro Javier Zapata*,† †

Department of Food Technology, School of Engineering of Orihuela (EPSO) and ‡Department of Applied Biology, School of Engineering of Orihuela (EPSO), University Miguel Hernández, Carretera de Beniel, km 3.2, 03312 Orihuela, Alicante, Spain ABSTRACT: The effects of methyl jasmonate (MeJa) treatment as an elicitor of artichoke plants [Cynara cardunculus var. scolymus (L.) Fiori] on the yield and quality attributes of artichokes, especially those related to individual phenolic content and antioxidant activity, at two harvest dates and along storage were analyzed in this research. Plants treated gave a higher yield of artichokes in comparison to control plants, with 0.55 kg more per plant. MeJa treatment also increased artichoke quality and phenolic content in the edible fraction at harvest and during storage at 2 °C for 28 days as a result of the accumulation of hydroxycinnamic acids and luteolin derivatives. In addition, antioxidant activity was enhanced by MeJa treatment and correlated with the total phenolic content. Results suggest that MeJa foliar application could be a simple and practical tool to improve the yield and phytochemical content on artichokes, with elicitation being a cheap and environmentally friendly procedure to improve the health-beneficial effects of artichoke consumption. KEYWORDS: preharvest treatment, postharvest quality, antioxidant activity, hydroxycinnamic acids, luteolin derivatives

■

INTRODUCTION The domesticated or globe artichoke [Cynara cardunculus var. scolymus (L.) Fiori], belonging to the family Asteraceae, is a traditionally consumed vegetable in the Mediterranean area. Artichoke production in Spain is almost exclusively based on the ‘Blanca de Tudela’ cultivar, which is propagated by striking and has excellent overall quality; however, its precocity and yield are lower than in seed-propagated cultivars.1 The edible fraction of artichoke plants includes the inner bracts and receptacle of the immature inflorescence, which constitutes nearly 35−55% of the fresh weight of the artichoke (or artichoke head), depending upon variety, development stage at harvest, and date of harvest.2 Apart from being consumed as a food, as fresh or processed product, artichoke is recognized as a herbal medicine.3,4 Thus, several in vitro and in vivo experiments have demonstrated the health-promoting effects of globe artichoke extracts, which have been attributed to the phenolic compounds present in leaves5−8 and artichoke heads.2,9−13 In comparison to other vegetables, artichoke contains high levels of total phenolics, mainly caffeoylquinic acids and luteolin glucosides, which have been related to its antioxidant properties.2,3,5,6,10,14 In addition, the level of phenolic compounds is influenced by cultivar, development stage at harvest, environmental conditions, and agronomic management.3,10,15−17 Biotic elicitors are plant molecules able to trigger plant defense responses, contributing to increase plant resistance against future pathogen attacks and also having the effect on improving the phytochemical composition of plants.18−20 In this sense, jasmonic acid is a plant elicitor playing key roles on activating different signaling pathways to synthesize the optimal mixture of defense metabolites.21 Moreover, treatments with exogenous jasmonic acid or methyl jasmonate (MeJa) can also stimulate pathogen-induced plant defense responses and lead to © 2017 American Chemical Society

production of bioactive secondary metabolites though several mechanisms.21 Thus, preharvest MeJa treatments increased bioactive compounds and antioxidant activity in plums,22 sweet cherry,23 black currants,24 raspsberries,25 apples,26 and grapewine27 as a result of enhanced phenylalanine ammonia-lyase (PAL) activity,28 improving quality and health properties of fresh fruit and vegetable consumption.29 However, to our knowledge, no publications are found in the literature regarding the effects of MeJa treatment of artichoke plants on the yield and quality of artichokes. Therefore, the aim of this paper was to evaluate the influence of MeJa foliar application to ‘Blanca de Tudela’ artichoke plants along the whole growth cycle on the yield and artichoke quality parameters at two harvest dates. In addition, the effect of preharvest MeJa treatments on the individual phenolic concentration and antioxidant activity along postharvest storage will be discussed.

■

MATERIALS AND METHODS

Plant Material and Treatments. For the experiment, the artichoke ‘Blanca de Tudela’ cultivar was used along the developmental cycle from August 2015 (when artichokes were sown) to April 29th, 2016 (when the last harvesting was made), in a commercial plot located at southern Spain (Alicante) under a Mediterranean climate. The soil type was clay loam with 15% clay, 45% sand, and 40% silt, which was treated with herbicide (before planting) and artichoke cuttings planted at 0.8 × 1.2 m. Fungicides and insecticides were applied along the growth cycle as necessary according to integrated production management. Fertilizers were applied in the drip irrigation system and were composed of 250N-120P-300K. The experiment was Received: Revised: Accepted: Published: 9247

July 25, 2017 September 26, 2017 September 29, 2017 September 29, 2017 DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry

10000g for 15 min at 4 °C. The supernatant was used for identification and quantification of individual phenolics in duplicate using HPLC− DAD−ESI/MSn and RP-HPLC−DAD systems, respectively. The injection volume was 8 μL, and chromatograms were recorded at 320 and 360 nm in an Agilent HPLC 1200 Infinity series, equipped with a photodiode array detector (Agilent Technologies, Waldbronn, Germany) and a mass detector in series (Bruker Daltonics Ultra HCT-ESI Ion Trap, Bremen, Germany). The column used was a Luna C18 column (250 × 40 mm, 5 mm particle size, Tenokroma, Barcelona, Spain). Mobile phases A and B were water/formic acid (99:1, v/v) and acetonitrile, respectively, with a flow rate of 0.8 mL/ min. The linear gradient started with 1% solvent B, reaching 15% solvent B at 15 min, 30% at 30 min, 40% at 50 min, 95% at 45 min, maintained to 50 min, and returning to 1% until 60 min. Collisioninduced fragmentation experiments were performed in the ion trap using helium as the collision gas, with voltage ramping cycles from 0.3 to 2 V. The mass spectrometry (MS) data were acquired in negative ionization mode for non-colored flavonoids. MSn was carried out in the automatic mode on the more abundant fragment ion in MS (n1). Individual phenolic compounds were identified by their mass in HPLC−DAD−ESI/MSn, their spectra, and retention times using previous bibliography. Moreover, some of them were corroborated using analytical standards (3-O-caffeoylquinic acid, 5-O-caffeoylquinic acid, 1,3-di-O-caffeoylquinic acid, and 3,5-di-O-caffeoylquinic acid). Luteolin derivatives were quantified using a calibration curve of quercetin 3-O-rutinoside at 360 nm, and hydroxycinnamic acids were quantified using 5-O-caffeoylquinic acid at 320 nm. Results are expressed as milligrams per 100 g. The total phenolic concentration was calculated as the sum of concentrations of individual phenolics. Antioxidant Activity. The total antioxidant activity (TAA) was measured from hydrophilic (H-TAA) and lipophilic (L-TAA) extracts and quantified as described in the study by Valero et al.33 by homogenizing 2 g of tissue sample with 5 mL of 50 mM Na phosphate buffer (pH 7.8) and 3 mL of ethyl acetate. After centrifugation, the upper and lower fractions were used for L-TAA and H-TAA quantification, respectively, using the enzymatic system composed of the chromophore 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), the horseradish peroxidase (HRP) enzyme, and its oxidant substrate [hydrogen peroxide (H2O2)], in which ABTS+ radicals are generated and monitored at 730 nm. Results are expressed as milligrams of Trolox equivalent per 100 g. Statistical Analysis. Results are expressed as the mean ± standard error (SE) of three replicates. For the field experiments, the Student’s t test was performed for each picking date to find significant differences at p < 0.05 between treatments, control and 0.5 mM MeJa. For postharvest storage experiments, data for the analytical determinations were subjected to analysis of variance (ANOVA). Sources of variation were storage time and treatment. Mean comparisons were performed using Duncan’s honest significant difference (HSD) test to examine if differences were significant at p < 0.05. All analyses were performed with SPSS software package version 12.0 for Windows.

randomly designed as blocks using three replicates of four rows with 32 plants in each of them, for each treatment (control and 0.5 mM MeJa). Tap water or freshly prepared 0.5 mM MeJa solution (previously dissolved in 10 mL of ethanol), both containing 0.5% Tween-20 as a surfactant, were foliar-sprayed with a mechanical mist sprayer and repeated each 21 days during the whole plant growth cycle: from T1 (October 12th, 45 days before the first harvesting) to T10 (April 18th, 11 days before the end cycle), using 30 L in each application. The applied MeJa concentration was chosen according to previously published papers, in which the concentration in the range of 0.1−2 mM was used.22−27 Artichoke Plant Yield, Measures of Quality Parameters, and Storage Experimental Design. Artichokes from control and treated plants were picked at the commercial development stage based on their size and morphology. A total of 15 harvestings were performed from November 26th to April 29th. Weight and number of artichokes harvested from each row were recorded, and then the number of artichokes harvested per plant, yield per plant, and artichoke weight were calculated. After that, artichokes were separated as first class (without visual defects and diameter higher than 80 mm) and second class (with slight visual defects and/or diameter lower than 80 mm) and the percentage of first and second class artichokes was calculated. Artichokes harvested on December 10th (which had received three MeJa treatments) and April 3rd (which had received nine MeJa treatments) and rated as first class were used to measure the respiration rate and quality parameters, including the individual phenolic concentration and antioxidant activity. For this purpose, about 2 kg of first class artichokes from each treatment and replicate were transported to the laboratory in 2 h. Then, one lot of three artichokes from each replicate and treatment was made at random in which the analytical determinations were performed. In addition, on December 10th, another three lots of three artichokes were made at random for each replicate and treatment, which were weighed and labeled, and then stored at 2 °C and 85% relative humidity in macroperforated plastic bags. After 14 and 28 days of cold storage, one lot of each replicate and treatment was taken at random in which the analytical determinations were made. Respiration Rate, Firmness, and Color. For the respiration rate, each of the three lots or replicates were deposited in 3.3 L jars and hermetically sealed for 30 min. After that, 1 mL from the jar atmosphere was withdrawn and used for injection into a gas chromatograph (Shimadzu, Kyoto, Japan) equipped with a thermoconductivity detector (GC−TCD) to quantify the CO2 concentration according to a previous report30 and the respiration rate (measured in duplicate in each replicate) was expressed as milligrams of CO2 per ́ kilogram per hour. For firmness determination, the protocol of RuizJiménez et al.30 was followed. In brief, firmness was measured twice independently in each artichoke of each replicate using a TX-XT2i texture analyzer (Stable Microsystems, Godalming, U.K.) and results were expressed as the force/deformation ratio (N mm−1). Color was measured in the outer bracts at three points around the equatorial external surface of each artichoke using a Minolta colorimeter (CRC200, Minolta Camera Co., Japan), and the CIELab coordinates of L*, a*, and b* parameters were recorded. Then, the greenest external bracts of each artichoke were removed, and a 5 mm slice of the edible fraction (internal bracts and receptacle) from each of the three artichokes of each replicate was taken. These slices were cut in small pieces and ground under liquid N2 to obtain a homogeneous sample of each replicate, in which individual phenolic compounds and antioxidant activity were measured, and in both cases, extractions were performed immediately. Identification of Phenolic Compounds by High-Performance Liquid Chromatography Coupled with Diode Array Detection and Electrospray Ionization Tandem Mass Spectrometry (HPLC−DAD−ESI/MSn) and Quantification by Reversed-Phase High-Performance Liquid Chromatography Coupled with Diode Array Detection (RP-HPLC−DAD). The protocol described by Gironés-Vilaplana et al.31 and adapted to artichoke32 was used. Briefly, 5 g samples from each replicate were homogenized with 15 mL of water/methanol (2:8) containing 2 mM NaF and centrifuged at

■

RESULTS AND DISCUSSION Field Results. Yield (g plant−1) was evaluated in all of the harvest dates, from November 26th, 2015 until April 29th, 2016, and results showed that, in most of them, MeJa treatment was effective on increasing the plant artichoke yield compared to controls (Figure 1). Two maximum production peaks were found (which are known as winter and spring peaks), and both occurred earlier in MeJa-treated plants than in control plants (Figure 1). This is an important issue, because artichokes that achieve a higher price at market are those harvested earlier.32 Taking into account all production data, it could be noticed that the crop yield was significantly increased by MeJa treatment, which was 3.75 ± 0.14 kg plant−1 in treated plants and 3.19 ± 0.16 kg plant−1 in controls. This effect was due to an increase on both the weight of artichoke (138 ± 1.15 and 144.7 ± 1.58 g in artichokes from control and MeJa-treated 9248

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry

date (≅3.5 N mm−1) with respect to the first harvest date (≅4.3 N mm−1) (Table 1). During cold storage, firmness decreased, reaching final values of ca. 3 N mm−1, which is attributed to a decrease in bract compactness during storage, mainly as a result of dehydration and bract opening, although no significant differences were found between control and treated artichokes (data not shown). The CIELAB parameters at harvest showed differences between artichokes harvested on December 10th and April 3rd, but not effect was observed as a result of the applied treatment. Artichoke heads from the first harvest date were darker than those from the second harvest date, which can be inferred from their lower values of L* and a* parameters and higher value of b* parameter (Table 1). On the other hand, no significant changes were observed in color parameters during 28 days of cold storage, on either control artichokes or treated artichokes (data not shown). With respect to weight loss, values at the end of storage were 5.53 ± 0.35% in control artichokes and significantly lower, 4.18 ± 0.21%, in treated artichokes. In this experiment, artichoke heads were stored in macroperforated plastic bags, and therefore, weight loss was lower than in previous experiments, in which the ‘Blanca de Tudela’ cultivar stored at 1 °C under open air reached ca. 28% of weight loss after 21 days32 and ca. 13% after 3 days at 20 °C.30 Phenolic Compounds. The HPLC−DAD−ESI/MS n analysis of the methanolic extracts of artichokes revealed seven hydroxycinnamic acids and three luteolin derivatives, which were identified and differentiated by MSn and retention time.32 The major phenolic compounds were 3,5-di-Ocaffeoylquinic acid (3,5-diCQA) and 5-O-caffeoylquinic acid (5-CQA, chlorogenic acid), with concentrations of 329.2 ± 7.8 and 242.9 ± 8.1 mg 100 g−1 in the edible portion of control artichokes harvested on December 10th (Figure 2), contributing to ca. 90% of the total phenolic content. On the other hand, 4,5-di-O-caffeoylquinic acid (4,5-diCQA), 3,4-di-Ocaffeoylquinic acid (3,4-diCQA), 1,3-di-O-caffeoylquinic acid (1,3-diCQA, cynarin), 3-O-caffeoylquinic acid (3-CQA, neochlorogenic acid), and 1-O-caffeoylquinic acid (1-CQA) were found at concentrations between 5 and 15 mg 100 g−1 (Figure 3). With regard to luteolin derivatives present in edible parts of artichoke heads, luteolin 7-O-glucoside was found at the highest concentration (ca. 20 mg 100 g−1 in control artichokes harvested on December 10th), followed by luteolin 7-Oglucuronide and luteolin 7-O-glucuronide 3-O-glucoside (Figure 4). The application of MeJa significantly induced the accumulation of these bioactive compounds in artichokes harvested on December 10th and April 3rd, although most of them were found at a lower concentration in the last harvest date (Figures 2−4). Thus, the total phenolic concentration (calculated as the sum of the individual concentrations) was 627.1 ± 10.3 and 502.5 ± 12.4 mg 100 g−1 in control artichokes

Figure 1. Artichoke yield (g plant−1), at several harvest dates, along the growth cycle (from November 26th to April 29th), in control and MeJa-treated plants. On top is indicated the dates of treatment. Data are the mean ± SE of three replicates (of four rows with 32 plants in each of them). For each picking date, bars with different letters show significant differences between control and treated plants (p < 0.05).

plants, respectively) and the number of artichokes per plant (23.12 ± 0.54 and 25.91 ± 0.39 in control and MeJa-treated artichoke plants, respectively). In addition, the percentage of first class artichokes was also higher in treated plants than in controls, with values of 35.75 ± 1.61 and 29.0 ± 1.3%, respectively. A limited number of papers are available regarding the effect of MeJa on vegetable product size, and contradictory results have been reported. Thus, preharvest treatments of plum trees with MeJa at 0.5 mM increased fruit size and weight in ‘Black Splendor’ and ‘Royal Rosa’ cultivars,22 while its application on vineyard did not affect berry weight.27 Respiration Rate and Quality Parameters. The respiration rate of artichoke heads was slightly lower in those from MeJa-treated plants than in those from control plants at both harvest dates, but the differences were no significant (Table 1). The respiration rate decreased when artichokes were stored at 2 °C in both control and treated artichokes, as a consequence of low-temperature storage, and no significant differences attributed to treatment could be found (data not shown). Similar firmness values were also obtained for control and MeJa-treated artichokes in both harvest dates, although firmness values were found to be lower in the second harvest

Table 1. Quality Parameters in Artichoke Harvested on December 10th or April 3rd as Affected by MeJa Treatmenta December 10th control respiration rate (mg of CO2 kg texture (N mm−1) color L* color a* color b* a

−1

−1

h )

120.44 4.30 56.99 −13.09 29.82

± ± ± ± ±

8.53 0.29 0.50 0.25 0.30

April 3rd

0.5 mM MeJa A A A A A

110.63 4.28 55.64 −13.42 29.67

± ± ± ± ±

10.20 A 0.21 A 0.56 A 0.22 A 0.27 A

control 125.25 3.56 58.28 −11.17 26.32

± ± ± ± ±

4.98 0.30 0.26 0.18 0.41

0.5 mM MeJa A A A A A

119.18 3.50 60.05 −10.34 26.65

± ± ± ± ±

6.83 0.18 0.38 0.26 0.29

A A B A A

For each parameter and harvest time, different letters show significant differences between control and MeJa-treated artichokes. 9249

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry

Figure 2. Concentration of major hydroxycinnamic acids on the edible portion of artichokes harvested on December 10th and stored for 14 and 28 days at 2 °C and in those harvested on April 3rd from control and MeJa (0.5 mM) preharvest treated plants. Data are the mean ± SE of three replicates. Bars with different letters show significant differences between control and treated artichokes for each sampling date (p < 0.05).

Figure 3. Concentration of minor hydroxycinnamic acids on the edible portion of artichokes harvested on December 10th and stored for 14 and 28 days at 2 °C and in those harvested on April 3rd from control and MeJa (0.5 mM) preharvest treated plants. Data are the mean ± SE of three replicates. Bars with different letters show significant differences between control and treated artichokes for each sampling date (p < 0.05).

9250

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry

Figure 4. Concentration of luteolin derivatives on the edible portion of artichokes harvested on December 10th and stored for 14 and 28 days at 2 °C and in those harvested on April 3rd from control and MeJa (0.5 mM) preharvest treated plants. Data are the mean ± SE of three replicates. Bars with different letters show significant differences between control and treated artichokes for each sampling date (p < 0.05).

Figure 5. (Left) Total phenolic content (TPC) and total antioxidant activity in the hydrophilic extracts (H-TAA) in the edible portion of artichokes harvested on December 10th and stored for 14 and 28 days at 2 °C and in those harvested on April 3rd from control and MeJa-treated plants and (right) linear correlation between TPC and H-TAA. For TPC and H-TAA, data are the mean ± SE of three replicates. Bars with different letters show significant differences between control and treated artichokes for each sampling date (p < 0.05).

still found at higher concentrations in artichokes from MeJatreated plants than in those from control plants (Figure 2−4). With regard to individual phenolic profile and concentrations, remarkable differences have been reported among artichoke cultivars or genotypes, part of the inflorescence, harvest season, soil type, and fertilizer application.3,17,34 For instance, 1,5-diCQA was the most abundant compound within the caffeoylquinic derivates, followed by 5-CQA, 3-CQA, and finally 1,3-diCQA in ‘Romolo’ and ‘Istar’ artichoke cultivars.35 Accordingly, 1,5-diCQA and 5-CQA were the predominant caffeoylquinic acids in ‘Violetto di Sicilia’, ‘Tando de Palermo’, and ‘Tema 2000’ artichoke cultivars.17,36,37 With respect to ‘Blanca de Tudela’ cultivar, it was previously reported that the main phenolic compounds were 5-CQA and 3,5-diCQA + 1,5diCQA, which eluted together and could not be separated using

harvested on December 10th and April 3rd, respectively, and 706.8 ± 9.5 and 599.6 ± 13.1 mg 100 g−1 in MeJa-treated plants. On a general basis, most of the hydroxycinnamic acids increased, as did the storage period, with the exception of the minor hydroxycinnamic acids, 1-CQA and 1,3-diCQA (Figure 2 and 3). In a similar way, an increase in luteonin derivative concentrations occurred along storage, especially in the major luteonin derivatives, luteloin 7-O-glucoside and luteolin 7-Oglucuronide (Figure 4), with the last luteonin derivative being identified in artichoke for the first time in our previous paper32 and confirmed in the present work. Nevertheless, it is important to note than the effect of MeJa treatment was also noticeable along storage, because after 14 and 28 days of cold storage, hydroxycinnamic acids and luteonin derivativess were 9251

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry HPLC−DAD−ultraviolet−visible (UV−vis).38 However, in the present paper, we used different mobile phases and gradient than in this previous works and individual phenolic compounds were identified by their mass in HPLC−DAD−ESI/MSn, their spectra, and retention times, according to Lombardo et al.,3 who achieved separation of 3,5-diCQA and 1,5-diCQA by their UV−vis and mass spectrometric data, based on the previous reports of Schütz et al.4 and Clifford et al.39 Recently and in agreement with the results of the present study, 5-CQA, 3,5diCQA, and 1,5-diCQA have been the main phenolic compounds identified in several cultivars of globe and wild artichoke.40,41 On the other hand, the extent to which 1,3diCQA features in the profile can be related to the amount of moisture present in the methanolic extraction solvent and artichoke, being relatively high when 60% aqueous methanol is used3 but much smaller when the artichoke has been freezedried and/or at least 70% aqueous methanol is used.34,35,38 In this sense, low methanol/high water contents are well-known to facilitate acyl migration, particularly of 1,5-diCQA, which rapidly transforms to more stable 1,3-diCQA without accumulating 1,4-diCQA, and yielding 1-CQA by partial hydrolysis.42 Moreover, other chlorogenic acid derivatives, such as succinic-acid-containing chlorogenic acids, FQA, and cis-CQA, have been reported in artichoke and botanically related species, as recently reviewed.43 However, none of these compounds were identified in the present research. TAA was measured in hydrophilic (H-TAA) and lipophilic (L-TAA) extracts of the edible portion of artichoke heads, and results showed than H-TAA was 4.5-fold higher than L-TAA. Thus, H-TAA was 337.4 ± 21.8 and 298.5 ± 10.2 mg 100 g−1 in control artichokes harvested on December 10th and April 3rd, respectively, while L-TAA values were 71.1 ± 6.5 and 68.4 ± 2.6 mg 100 g−1, respectively. No significant changes were observed in L-TAA along storage, and no significant differences were found attributed to MeJa treatment (data not shown). On the contrary, H-TAA increased along storage, in both control and MeJa-treated artichokes, although it was significantly higher in the last artichokes, as well as total phenolic concentration, and a high correlation (r2 = 0.958) was found between them (Figure 5). Thus, phenolic compounds are the main compounds responsible for TAA in artichokes, according to previous reports in artichokes and fruits.17,32,33,44 In fact, the antioxidant potential of artichoke is mainly related to the antioxidant properties of polyphenols, because they have powerful antioxidant activities, being able to scavenge a wide range of reactive oxygen species (ROS), such as superoxide, hydroxyl, and peroxyl radicals, and are also able to chelate metal ions.28,41 In the present study, the relationship between H-TAA and the phenolic concentration and the effect of MeJa on enhancing both of them could be mainly attributed to the increases on the major phenolic compounds, 5-CQA and 3,5diCQA (Figure 2). This fact is of particular importance because it has been recently reported that these hydroxycinnamic acids have the highest bioaccesibility and bioavailability among the phenolic compounds in artichokes.17,45 In addition, artichoke extract showed higher antioxidant activity than the individual polyphenols, even after in vitro gastrointestinal digestion, which did not modify the antioxidant activity of artichoke polyphenols, except for 1,5-diCQA, which proved to be the least active.41 In this sense, it is worth mentioning that the effect of MeJa treatment on increasing hydroxyicinnamic acid and luteolin derivative concentrations in artichokes at harvest and during

storage would lead to an increase in the health-beneficial effects of artichoke consumption, because these compounds are responsible for its hepatoprotective, diuretic, antibacterial, anti-HIV, and anticarcinogenic effects as well as for its ability to inhibit cholesterol biosynthesis and low-density lipoprotein (LDL) oxidation.2,5−9,46 There are not previous reports regarding the effect of MeJa treatment of artichoke plants on phenolics of artichoke head, although some recent information exists on other crops. Thus, preharvest MeJa treatment increased anthocyanin and flavonoid contents in raspberries,25 apples,26 and black currants24 as well as the total phenolic content in both grape and wine,27,47,48 sweet cherries,23 and plums, which were maintained after prolonged cold storage.22,44 The effect of MeJa treatment on increasing the phenolic content could be attributed to its role as an elicitor through activation of the phenylpropanoid pathway, which is one of the inducible defense responses leading to accumulation of phenolic compounds and, therefore, to improve health benefits of artichoke consumption. However, Moglia et al.28 did not observed any effect of 0.1 mM MeJa treatment of leaf artichoke discs on the phenolic concentration after 24 h. Authors argued that probably a higher MeJa concentration would have been required to upregulate the phenylpropanoid biosynthesis. Overall results show for the first time that MeJa treatments applied to ‘Blanca de Tudela’ artichoke plants along the whole growth cycle increased yield and percentage of first class artichokes as well as the content of individual phenolic compounds in the edible fraction of artichokes at time of harvest. In addition, these bioactive compounds were maintained at higher concentrations in artichokes from MeJatreated plants than in those from controls after 28 days of cold storage, leading to artichokes with higher antioxidant activity. Although this experiment was performed using a single artichoke variety, both control and MeJa-treated plants were under similar agronomical and environmental conditions and a great number of artichoke plants were used (384 plants grouped in three replicates of 128 plants for each treatment), and in turn, results have significant relevance. Thus, MeJa could be considered as a good elicitor to improve quality and enhance the health-beneficial properties of artichoke consumption.

■

AUTHOR INFORMATION

Corresponding Author

*Telephone: +34-96-674-9789. Fax: +34-96-674-9677. E-mail: [email protected]. ORCID

Pedro Javier Zapata: 0000-0002-8715-8278 Notes

The authors declare no competing financial interest.

■ ■

ACKNOWLEDGMENTS The authors express their gratitude to OLÉ S.A.T. 9890 for providing the experimental farm and technical advice. REFERENCES

(1) Food and Agriculture Organization of the United Nations (FAO). Food and Agriculture Organization Corporate Statistical Database (FAOSTAT); FAO: Rome, Italy, 2012; http://faostat.fao. org/site/567/DesktopDefault.aspx?PageID=567#ancor (accessed March 15, 2017). (2) Lattanzio, V.; Kroon, P. A.; Linsalata, V.; Cardinali, A. Globe artichoke: A functional food and source of nutraceutical ingredients. J. Funct. Foods 2009, 1, 131−144.

9252

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry (3) Lombardo, S. A.; Pandino, G. A.; Mauromicale, G.; Knödler, M.; Carle, R.; Schieber, A. Influence of genotype, harvest time and plant part on polyphenolic composition of globe artichoke [Cynara cardunculus L. var. scolymus (L.) Fiori]. Food Chem. 2010, 119, 1175−1181. (4) Schütz, K.; Muks, E.; Carle, R.; Schieber, A. Quantitative determination of phenolic compounds in artichoke based dietary supplements and pharmaceuticals by high-performance liquid chromatography. J. Agric. Food Chem. 2006, 54, 8812−8817. (5) Brown, J. E.; Rice-Evans, C. A. Luteolin-rich artichoke extracts protects low density lipoproteins from oxidation in vitro. Free Radical Res. 1998, 29, 247−255. (6) Gebhardt, R. Antioxidative and protective properties of extracts from leaves of the artichoke (Cynara scolymus L.) against hydroperoxide-induced oxidative stress in cultured rat hepatocytes. Toxicol. Appl. Pharmacol. 1997, 144, 279−86. (7) Pérez-García, F.; Adzet, T.; Cañigueral, S. Activity of artichoke leaf extract on reactive oxygen species in human leukocytes. Free Radical Res. 2000, 33, 661−5. (8) Zapolska-Downar, D.; Zapolski-Downar, A.; Naruszewicz, M.; Siennicka, A.; Krasnodebska, B.; Kolodziej, B. Protective properties of artichoke (Cynara scolymus) against oxidative stress induced in cultured endothelial cells and monocytes. Life Sci. 2002, 71, 2897− 2908. (9) Lattanzio, V.; Cardinali, A.; Di Venere, D.; Linsalata, V.; Palmieri, S. Browning phenomena in stored artichoke (Cynara scolymus L.) heads: Enzymic or chemical reactions? Food Chem. 1994, 50, 1−7. (10) Lattanzio, V.; Van Sumere, C. F. Changes in phenolic compounds during the development and cold storage of artichoke (Cynara scolymus L.) heads. Food Chem. 1987, 24 (1), 37−50. (11) Schütz, K.; Kammerer, D.; Carle, R.; Schieber, A. Identification and quantification of caffeoylquinic acids and flavonoids from artichoke (Cynara scolymus L.) heads, juice, and pomace by HPLCDAD-ESI/MSn. J. Agric. Food Chem. 2004, 52, 4090−4096. (12) Llorach, R.; Espín, J. C.; Tomás-Barberán, F. A.; Ferreres, F. Artichoke (Cynara scolymus L.) byproducts as a potential source of health-promoting antioxidant phenolics. J. Agric. Food Chem. 2002, 50, 3458−64. (13) Brat, P.; Georgè, S.; Bellamy, A.; Du Chaffaut, L.; Scalbert, A.; Mennen, L.; Arnault, N.; Amiot, M. J. Daily polyphenol intake in France from fruit and vegetables. J. Nutr. 2006, 136, 2368−2373. (14) Clifford, M. N. Chlorogenic acids and other cinnamates Nature, occurrence and dietary burden. J. Sci. Food Agric. 1999, 79, 362−372. (15) Pandino, G.; Lombardo, S.; Mauromicale, G. Globe artichoke leaves and floral stems as a source of bioactive compounds. Ind. Crops Prod. 2013, 44, 44−49. (16) Pandino, G.; Courts, F. L.; Lombardo, S.; Mauromicale, G.; Williamson, G. Caffeyolquinic acids and flavonoids in the immature inflorescence of globe artichoke, wild cardoon, and cultivated cardoon. J. Agric. Food Chem. 2010, 58, 1026−1031. (17) Lombardo, S.; Pandino, G.; Mauromicale, G. The nutraceutical response of two globe artichoke cultivars to contrasting NPK fertilizer regimes. Food Res. Int. 2015, 76, 852−859. (18) Angelova, Z.; Georgiev, S.; Roos, W. Elicitation of plants. Biotechnol. Biotechnol. Equip. 2006, 20, 72−83. (19) Poulev, A.; O’Neal, J. M.; Logendra, S.; Pouleva, R. B.; Timeva, V.; Garvey, A. S.; Gleba, D.; Jenkins, I. S.; Halpern, B. T.; Kneer, R.; Cragg, G. M.; Raskin, I. Elicitation, a new window into plant chemodiversity and phytochemical drug discovery. J. Med. Chem. 2003, 46, 2542−2547. (20) Delaunois, B.; Jeandet, P.; Clément, C.; Baillieul, F.; Dorey, S.; Cordelier, S. Uncovering plant-pathogen crosstalk through apoplastic proteomic studies. Front. Plant Sci. 2014, 5, 249. (21) Creelman, R. A.; Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48, 355−381. (22) Martínez-Esplá, A.; Zapata, P. J.; Castillo, S.; Guillén, F.; Martínez-Romero, D.; Valero, D.; Serrano, M. Preharvest application

of methyl jasmonate (MeJA) in two plum cultivars. 1. Improvement of fruit growth and quality attributes at harvest. Postharvest Biol. Technol. 2014, 98, 98−105. (23) Castillo, S.; Valverde, J. M.; Guillén, F.; Zapata, P. J.; Díaz-Mula, H. M.; Valero, D.; Martínez-Romero, D.; Serrano, M. Methyl jasmonate and methyl salicylate affect differentially the postharvest ripening process of ’Primulat’ Sweet cherry. Acta Hortic. 2015, 1079, 541−544. (24) Flores, G.; Ruiz Del Castillo, M. L. Accumulation of anthocyanins and flavonols in black currants (Ribes nigrum L.) by pre-harvest methyl jasmonate treatments. J. Sci. Food Agric. 2016, 96, 4026−31. (25) Flores, G.; Ruiz Del Castillo, M. L. Variations in ellagic acid, quercetin and myricetin in berry cultivars after preharvest methyl jasmonate treatments. J. Food Compos. Anal. 2015, 39, 55−61. (26) Ozturk, B.; Yıldız, K.; Ozkan, Y. Effects of pre-harvest methyl jasmonate treatments on bioactive compounds and peel color development of “Fuji” apples. Int. J. Food Prop. 2015, 18, 954−962. (27) Portu, J.; Santamaría, P.; López-Alfaro, I.; López, R.; GardeCerdán, T. Methyl jasmonate foliar application to Tempranillo vineyard improved grape and wine phenolic content. J. Agric. Food Chem. 2015, 63, 2328−2337. (28) Moglia, A.; Lanteri, S.; Comino, C.; Acquadro, A.; de Vos, R.; Beekwilder, J. Stress-induced biosynthesis of dicaffeoylquinic acids in globe artichoke. J. Agric. Food Chem. 2008, 56, 8641−8649. (29) Reyes-Díaz, M.; Lobos, T.; Cardemil, L.; Nunes-Nesi, A.; Retamales, J.; Jaakola, L.; Alberdi, M.; Ribera-Fonseca, A. Methyl jasmonate: An alternative for improving the quality and health properties of fresh fruits. Molecules 2016, 21, 567. (30) Ruíz-Jiménez, J. M.; Zapata, P. J.; Serrano, M.; Valero, D.; Martínez-Romero, D.; Castillo, S.; Guillén, F. Effect of oxalic acid on quality attributes of artichokes stored at ambient temperature. Postharvest Biol. Technol. 2014, 95, 60−63. (31) Gironés-Vilaplana, A.; Valentão, P.; Moreno, D. A.; Ferreres, F.; García-Viguera, C.; Andrade, P. B. New beverages of lemon juice enriched with the exotic berries maqui, açai,́ and blackthorn: Bioactive components and in vitro biological properties. J. Agric. Food Chem. 2012, 60, 6571−6580. (32) Martínez-Esplá, A.; García-Pastor, M. E.; Zapata, P. J.; Guillén, F.; Serrano, M.; Valero, D.; Gironés-Vilaplana, A. Preharvest application of oxalic acid improves quality and phytochemical content of artichoke (Cynara scolymus L.) at harvest and during storage. Food Chem. 2017, 230, 343−349. (33) Valero, D.; Díaz-Mula, H. M.; Zapata, P. J.; Castillo, S.; Guillén, F.; Martínez-Romero, D.; Serrano, M. Postharvest treatments with salicylic acid, acetylsalicylic acid or oxalic acid delayed ripening and enhanced bioactive compounds and antioxidant capacity in Sweet cherry. J. Agric. Food Chem. 2011, 59, 5483−5489. (34) Lombardo, S.; Pandino, G.; Ierna, A.; Mauromicale, G. (2012). Variation of polyphenols in a germplasm collection of globe artichoke. Food Res. Int. 2012, 46, 544−551. (35) Rouphael, Y.; Colla, G.; Graziani, G.; Ritieni, A.; Cardarelli, M.; De Pascale, S. Phenolic composition, antioxidant activity and mineral profile in two seed-propagated artichoke cultivars as affected by microbial inoculants and planting time. Food Chem. 2017, 234, 10−19. (36) Pandino, G.; Lombardo, S.; Mauromicale, G.; Williamson, G. Profile of polyphenols and phenolic acids in bracts and receptacles of globe artichoke (Cynara cardunculus var. scolymus) germplasm. J. Food Compos. Anal. 2011, 24, 148−153. (37) Pandino, G.; Lombardo, S.; Antonino, L. M.; Ruta, C.; Mauromicale, G. In vitro micropropagation and mycorrhizal treatment influences the polyphenols content profile of globe artichoke under field conditions. Food Res. Int. 2017, 99, 385−392. (38) Gil-Izquierdo, A.; Conesa, M. A.; Ferreres, F.; Gil, M. I. Influence of modified atmosphere packaging on quality, vitamin C and phenolic content of artichokes (Cynara scolymus L.). Eur. Food Res. Technol. 2002, 215, 21−27. 9253

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254

Article

Journal of Agricultural and Food Chemistry (39) Clifford, M. N.; Knight, S.; Kuhnert, N. Discriminating between the six isomers of dicaffeoylquinic acid by LC-MSn. J. Agric. Food Chem. 2005, 53, 3821−3832. (40) Petropoulos, S. A.; Pereira, C.; Ntatsi, G.; Danalatos, N.; Barros, L.; Ferreira, I. C. F. R. Nutritional value and chemical composition of Greek artichoke genotypes. Food Chem. 2017, DOI: 10.1016/ j.foodchem.2017.01.159. (41) Garbetta, A.; Capotorto, I.; Cardinali, A.; D’Antuono, A.; Linsalata, V.; Pizzi, F.; Minervini, F. Antioxidant activity induced by main polyphenols present in edible artichoke heads: Influence of in vitro gastro-intestinal digestion. J. Funct. Foods 2014, 10, 456−464. (42) Clifford, M. Some Notes on the Chlorogenic Acids. 3. LC and LC− MS. Version 3 January 2017; University of Surrey: Surrey, U.K., 2018; DOI: 10.13140/RG.2.2.10825.95844. (43) Clifford, M. Some Notes on the Chlorogenic Acids. Part 4. Botanical Distribution of the Chlorogenic Acids Version 1 January 2017; University of Surrey: Surrey, U.K., 2017; DOI: 10.13140/ RG.2.2.23428.53126. (44) Zapata, P. J.; Martínez-Esplá, A.; Guillén, F.; Díaz-Mula, H. M.; Martínez-Romero, D.; Serrano, M.; Valero, D. Preharvest application of methyl jasmonate (MeJA) in two plum cultivars. 2. Improvement of fruit quality and antioxidant systems during postharvest storage. Postharvest Biol. Technol. 2014, 98, 115−122. (45) D’Antuono, I.; Garbetta, A.; Linsalata, V.; Minervini, F.; Cardinali, A. Polyphenols from artichoke heads (Cynara cardunculus (L.) subsp. scolymus Hayek): In vitro bio-accessibility, intestinal uptake and bioavailability. Food Funct. 2015, 6, 1268−1277. (46) Seelinger, G.; Merfort, I.; Wölfle, U.; Schempp, C. M. Anticarcinogenic effects of the flavonoid luteolin. Molecules 2008, 13, 2628−2651. (47) Ruiz-García, Y.; Romero-Cascales, I.; Gil-Muñoz, R.; FernándezFernández, J. I.; López-Roca, J. M.; Gómez-Plaza, E. Improving grape phenolic content and wine chromatic characteristics through the use of two different elicitors: Methyl jasmonate versus benzothiadiazole. J. Agric. Food Chem. 2012, 60, 1283−1290. (48) Fernández-Marín, M. I.; Puertas, B.; Guerrero, R. F.; GarcíaParrilla, M. C.; Cantos-Villar, E. Preharvest methyl jasmonate and postharvest UVC treatments: Increasing stilbenes in wine. J. Food Sci. 2014, 79, C310−C317.

9254

DOI: 10.1021/acs.jafc.7b03447 J. Agric. Food Chem. 2017, 65, 9247−9254