Grafting Influences Phenolic Profile and Carpometric Traits of Fruits of

Article pubs.acs.org/JAFC

Grafting Influences Phenolic Profile and Carpometric Traits of Fruits of Greenhouse-Grown Eggplant (Solanum melongena L.) Nina Kacjan Maršić,* Maja Mikulič-Petkovšek, and Franci Štampar Biotechnical Faculty, Department of Agronomy, Chair for Fruit, Wine and Vegetable Growing, University of Ljubljana, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia ABSTRACT: The influence of eggplant grafting on tomato rootstock was evaluated during the two growing seasons. Yield, quality traits, and individual phenolics in fruits were assessed. Three commercial varieties and one landrace were used as scions. Grafting significantly increased eggplant yield and decreased the presence of calyx prickles. The effect of grafting on the accumulation of major phenolic constituents in eggplant fruit was inconsistent: in the year with less solar radiation and lower mean daily air temperatures, grafting decreased phenolic content in commercial variety/rootstock fruit and increased the content in landrace/rootstock fruit. An opposite effect in the latter combination was observed in the year with improved conditions for eggplant cultivation. The browning potential of fruit pulp was highly dependent on variety/landrace and partly also on grafting combination. Differences in correlations between phenolic constituents and browning potential (positive for varieties and negative for landrace) could also be ascribed to the importance of other antioxidants for diminished eggplant pulp browning. KEYWORDS: eggplant, grafting, scion/rootstock combination, phenolic acids, quercetin glycosides, flavonols, anthocyanins

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INTRODUCTION Eggplant (Solanum melongena L.) is a warm-weather crop originating from Asia and is cultivated mostly in tropical and temperate regions.1 Compared to other Solanaceous crops, such as tomato or bell pepper, eggplant is well-adapted to high rainfall and high temperatures and is capable of producing a high yield in hot−wet environments.2 In Europe, southern Italy is the top producer of eggplant, and its production mainly takes place in open fields during the spring−summer period or in greenhouses from September to harvesting in December.3 In the Mediterranean region, eggplants are cultivated in greenhouses, mainly for out-of-season production, when market prices are high.4 Continuous cropping is inevitable with intensive protected cultivation, and consequently, soil infections often occur.5 Many commercial eggplant varieties are susceptible to biotic and abiotic stresses,6 so eggplant grafting on resistant rootstocks has been used and found to be effective for inducing resistance to soilborne pathogens and other stress situations.3,7−9 Grafting offers not only productive advantages but also the alteration of some quality traits of the fruit, which are of great importance for fruit marketability and consumer preferences.10,11 Eggplant produces fruits with many different shapes (ovoid, oblong, cylindrical, club shape), sizes, and colors (purple, green, purple with white stripes), depending on the variety. The oblong to elongated purple/black eggplant is used worldwide, but varieties also differ in their spiny or nonspiny calyx. Most of the visual characteristics of eggplant fruits are highly genetically influenced.12 In addition to the morphologic features of fruit, the composition of phytochemicals is of great importance, especially those with antioxidant properties.13 Eggplant is among the top 10 vegetables in terms of oxygen radical absorbance capacity (ORAC), and this trait is attributed to its high level of phenolic antioxidants.14 Many of them have been found to have strong anticancer and anti-inflammation activity.15,16 However, a drawback © 2014 American Chemical Society

of the higher level of phenolics in eggplant fruits is that the oxidation of phenolics causes the browning of the fruit pulp after its exposure to the air, and this may lead to a reduction in the apparent quality.17 The varieties of eggplant differ also with respect to the extent of postcutting browning, which could be due to variations in the polyphenol oxidase activity, the level of soluble phenolics in eggplant pulp,18 or the presence some other antioxidants, such as ascorbic acid, which has antibrowning properties. Phenolic compounds are found in the pulp and eggplant peel19−21 and are significantly influenced by genotype,12,22,23 environment and soil type,24 and growth and storage conditions,25 as well as by cultivation systems26−28 and grafting.1,3 However, the majority of these studies did not assess the level of individual polyphenols but expressed them as total phenolic content, using various methods, and the results thus showed large differences in values, probably reflecting different extraction methods, plant varieties, growing regions, soil type, and duration of light exposure.29 The composition of individual phenolics has been reported in very few studies. These have shown that, based on molecular structure, phenolics in the pulp and peel of purple eggplant varieties are divided into three major groups: hydroxycinnamic acids, flavonols, and anthocyanins.21,28 Despite the fact that there have been some reports of the grafting effect on the concentration of total phenolic content in eggplant fruit,3,8 few details are known about the variation of individual phenolic concentrations in eggplant fruit in relation to grafted and self-grafted plants. In the present study, changes of a wide range of phenolics in the fruits of three commercial varieties and one landrace of purple eggplant grafted onto tomato rootstock during two Received: Revised: Accepted: Published: 10504

July 12, 2014 October 1, 2014 October 2, 2014 October 2, 2014 dx.doi.org/10.1021/jf503338m | J. Agric. Food Chem. 2014, 62, 10504−10514

Journal of Agricultural and Food Chemistry

Article

Table 1. Eggplant Scion and Rootstock Varieties Included in the Experiments plant material

code

commercial varieties Blackbell F1 Epic F1 Galine F1 landrace Domači srednje dolgi rootstock Beaufort F1 (S. lycopersicum L. × S. habrochaites)

fruit shape or characteristics

seed company

country of origin

BB EC GA

elongated oval cylindrical round oval

Petoseed Petoseed Clause

USA USA France

DSD

round flask

Semenarna Ljubljana

Slovenia

BE

cold tolerant root system with strong branching, resulting in a very strong plant

De Ruiter

Holland

Table 2. Monthly Meteorological Data from May to September of 2010 and 2011 from Ljubljana Meteorological Station on the Experimental Field of the Biotechnical Faculty, University of Ljubljanaa year 2010

year 2011

month

TS

TOD

TX

TM

MSR

TS

TOD

TX

TM

MSR

MRS

May June July August September

15.3 20.3 22.9 20.3 14.7

0.7 2.5 3.0 1.2 −0.8

19.8 25.5 28.9 26.0 19.2

11.2 14.5 17.3 15.5 11.3

14.5 19.4 20.6 16.9 10.5

17.0 20.0 21.1 22.8 19.4

2.4 1.1 1.2 3.7 3.9

23.6 25.5 26.9 29.5 26.4

9.5 14.7 15.3 16.2 13.7

22.6 20.2 20.9 21.0 15.4

19.1 20.3 20.1 17.3 13.0

a TS, mean monthly air temperature (°C); TOD, temperature deviation from the 1961−1990 average (°C); TX, mean maximum air temperature for the month (°C); TM, mean minimum air temperature for the month (°C); MSR, mean daily solar radiation (MJ m−2); MSR, average of the mean daily solar radiation (MJ m−2) for the period 1961−1990.

0−0.3 m soil layer. At the beginning of the season, the average initial soil nitrate content was 5.2 mg kg−1 for the same depth, soil assimilable P and K was 22 and 28 mg kg−1, respectively, on the basis of which application rates of macronutrients were calculated according to the Regulations on Integrated Production of Vegetables. One day before transplanting, granulated mineral fertilizers were incorporated on the plots at a rate of 70 kg N ha−1, 50 kg P ha−1 and 235 kg K ha−1, and 20 kg Ca ha−1 as calcium ammonium nitrate, super phosphate, and potassium sulfate, respectively. The remaining N and Ca (150 and 184 kg ha−1) were applied via fertigation with the water-soluble fertilizer (WSF) calcium nitrate (Multi-Cal, Haifa Chemicals, Israel). Irrigation was applied as required through a drip tape (T-tape TSX 500 model, T-systems International) beneath the plastic mulch. Diseases were managed with applications of Vertimec (Syngenta Agro d.o.o., Ljubljana, Slovenia) (0.05% on July 11, 2010 and on July 4, 2011) and Calipso SC 480 (Bayer Ag., Leverkusen, Germany) (0.03% on July 27, 2011). Weather Conditions. Average daily temperature and total daily solar irradiation (presented in Table 2) during the experimental period from May to September of 2010 and 2011 were taken from the meteorological station on the experimental field of the Biotechnical Faculty in Ljubljana, Slovenia. It can be assumed that the environmental conditions in the greenhouse were very similar to those in the open field but, on the basis of experience from previous years, 3−4 °C higher. The weather during the experimental period in 2010 was comparable to the long-term average, but the average daily temperatures were slightly above the long-term average, with the highest positive deviation in June (by 2.5 °C) and in July (by 3 °C), while the average daily temperature in September fell below the long-term average daily temperature by 0.8 °C. The year 2011 was comparable to the long-term average in terms of temperature. Higher temperatures compared to the long-term average (more than 3 °C higher) were measured in May, August, and September. More solar radiation compared to the long-term average was measured in all months during the experimental period in both years. The highest monthly averages of total daily solar radiation in 2010 were in June and July, 27 and 15% above the long-term average, respectively. Higher than average solar radiation was recorded in 2011, being highest in May (58%), August (45%), and September (55%).

growing season are reported. All phenolic compounds were confirmed using a mass spectrometer with an electrospray interface (ESI) operating in negative ion mode. The results provide information on the advantages of grafted eggplant fruit, which are recognized in the outer and inner quality parameters and are important from the point of view of the consumer as well as the vegetable producer. Knowing the effect of grafting on important fruit quality traits, especially changes in the phenolic profile, could also be very helpful for rootstock breeders, who have stressed the market value of fruits of grafted plants as a focus of most rootstock breeding efforts.7

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MATERIALS AND METHODS

Plant Material. Fruits were collected from three commercial varieties of eggplant, Blackbell F1 (BB), Epic F1 (EC), Galine F1 (GA), and landrace Domači srednje dolgi (DSD), which had been grafted onto tomato rootstock Beaufort F1 (BE) (and self-grafted plants were used as a control) using the cleft procedure described by Lee30 and were grown in experiments from May until September in 2010 and 2011, on the experimental field (latitude 46°2′, longitude 14°28′, 298 m asl) of the Biotechnical Faculty in Ljubljana, Slovenia. The main characteristics of each of the varieties are presented in Table 1. Successfully grafted plants were transplanted on May 24 in both years at a planting density of 0.8 × 0.8 m2 (plant density of 12 500 plants ha−1) in an unheated three-span greenhouse with flap ventilation at the ridge and roll-up ventilation at the side walls. Each span was 6 m wide and 25 m long and covered with a transparent polycarbonate Lexan corrugated sheet (LCS100, SABIC Innovative Plastics, Netherlands), with 89% visible light transmittance and 30)], as well as color measurement and polyphenolic content, was studied on these samples. Color Measurements. Skin color measurements were conducted to confirm skin color uniformity within individual varieties and among them in order to eliminate the effect of skin color as a factor that could influence the chemical composition of anthocyanins. Skin color was measured on the equatorial region of the fruits using a Minolta CR 300 Chroma portable colorimeter (Minolta Co., Osaka, Japan) with C illuminant for each fruit, and an average for individual varieties was calculated. Fruit chromaticity was expressed in L*, a*, b* color space coordinates (CIELAB). Color was described by the CIRG index, specifically intended for the evaluation of the external color of violet-colored fruits31 and calculated as (180 − h)/[L* + √(a2 + b2)], where h represents the hue angle. Determination of Browning. Fruit flesh color was measured using the same colorimeter (Minolta CR 300) to determine the lightness of fruit pulp by measuring the L* value (0 = black, 100 = white). Fruit was cut transversally at the midpoint between the blossom and stem ends, and measurements were made on the surface immediately after being cut, 10 min later, and after 30 min, when maximum browning was achieved. The oxidation potential was estimated using the method of Larrigaudiere et al.32 with a slight modification as suggested by Concellon et al.25,33 A colorimeter was used to measure the color parameter L* on the section obtained, as described earlier. Measurements obtained immediately after cutting were marked L0, those obtained after 10 min were marked L10, and those after 30 min were marked L30. The browning potential was expressed as ΔL10 = (L0 − L10) and ΔL30 = (L30 − L0). Chemicals. The standards used to determine the phenolic compounds in samples were chlorogenic acid (5-caffeoylquinic acid) and quercetin 3-O-rutinoside from Sigma-Aldrich and (−)-epicatechin, (+)-catechin, delphinidine, quercetin 3-O-rhamnoside, quercetin-3-Ogalactoside, and quercetin 3-O-glucoside from Fluka Chemie (Buchs, Switzerland). Methanol for extraction of phenolics was acquired from Sigma-Aldrich. The chemicals for the mobile phases were HPLC− MS-grade acetonitrile and formic acid from Fluka. Water for the mobile phase was double distilled and purified with the Milli-Q system (Millipore, Bedford, MA) Extraction and HPLC−MS/MS Identification of Phenolic Compound. The eggplant fruits were peeled with a mechanical peeler and the peel was separated from the pulp. The extraction of fruit samples (peel and pulp separately) was done as described by Mikulic-Petkovsek et al.34 with some modification. Fresh eggplant samples were ground to a fine powder in a mortar chilled with liquid nitrogen. The samples of 10 g of pulp or 5 g of peel were extracted with 10 mL of methanol containing 3% (v/v) formic acid and 3% (w/v) 2,6-di-tert-butyl-4-methylphenol (BHT) in a cooled ultrasonic bath for 1 h. BHT was added to the samples in order to prevent oxidation. After extraction, the fruit extracts were centrifuged for 7 min at 10 000 rpm. The supernatant was filtered through a Chromafil AO-45/25 polyamide filter produced by Macherey-Nagel and transferred to a vial prior to injection into the HPLC system. The individual phenolic compounds were analyzed using the Thermo Finnigan Surveyor HPLC system (Thermo Scientific, San Jose, CA) with a diode array detector at 280 nm (flavanols, cinnamic acid derivatives), 350 nm (flavonols), and 530 nm (anthocyanins). A Phenomenex (Torrance, CA) HPLC column C18 (150 × 4.6 mm, Gemini 3 μm) protected with a Phenomenex Security guard column and operated at 25 °C was used for the separation of

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RESULTS Data for yield, expressed as the number of fruits per plant, and other visible fruit traits, such as fruit weight, color, and shape, as well as fruit calyx prickles, for the eggplant varieties grafted onto tomato rootstock are presented in Table 3. For the number of fruits per plant, both main effects (rootstock and variety) were significant (p = 0.001) in both years, while the interaction between them (p = 0.01) was significant only in 2011. In 2010, grafting significantly increased the number of fruits per plant for all varieties, while in 2011 the same effect of grafting was found with two varieties and landrace but not with GA. The significant effect of variety on fruit yield was also confirmed by ANOVA (p = 0.001), with a significantly higher number of fruits per plant for all commercial varieties compared to landrace DSD. For the average fruit weight, ANOVA showed a significant impact of variety (p = 0.001) in 2010, while in 2011 both main effects were significant, as was also their interaction. In the first year, heavier fruits were recorded with BB and DSD compared to EC and GA, while between them no significant differences were found (Table 2). In the second year, grafting increased the average fruit weight with GA, EC, and DSD compared to self-grafted plants, but the differences were significant only with landrace DSD (p = 0.01). For the color index CIRG, ANOVA showed a significant impact of varieties in both years, and in 2011 the V × T 10506

dx.doi.org/10.1021/jf503338m | J. Agric. Food Chem. 2014, 62, 10504−10514


Article

Table 3. Visible Quality Traits of Three Commercial Eggplant Varieties (BB, EC, GA) and One Eggplant Landrace (DSD) Grafted onto Tomato Rootstock (Rs) and Self-Grafted (Sg)a year

variety

2010

BB

number of fruit per plant

fruit weight (g)

CIRG

fruit length/width ratio

fruit calyx prickles (scale 0−9)

8.5 6.4 5.8 4.1 8.6 7.1 9.2 6.8

238.2 236.4 246.8 239.4 208.6 202.4 224.7 196.8

6.8 6.6 6.7 6.5 7.1 7.0 6.9 6.5

1.62 1.72 1.29 1.36 2.08 2.14 1.70 1.80

2.33 3.00 1.17 3.67 1.00 2.00 1.67 2.67

sign.b

V (SEc) T (SE) V × T (SE) BB DSD EC GA Rs Sg

*** (0.39) *** (0.27) NS 7.4 ab 4.9 b 7.8 a 8.0 a 8.1 a 6.1 b

*** (9.47) NS NS 237.2 a 243.0 a 205.1 b 210.2 b 177.7 217.5

** (0.08) NS NS 6.7 b 6.6 b 7.0 a 6.7 b 6.8 6.7

*** (0.05) NS NS 1.67 ab 1.32 b 2.11 a 1.75 ab 1.67 1.75

** (0.23) *** (0.16) NS 2.67 a 2.42 a 1.51 b 2.17 ab 1.54 a 2.83 b

BB

Rs Sg Rs Sg Rs Sg Rs Sg

7.9 bc 3.3 e 9.4 ab 4.8 d 10.1 a 7.1 c 7.3 c 6.9 c

276.7 299.3 256.9 197.1 249.4 231.9 245.2 218.8

8.6 6.5 5.3 6.1 5.5 7.1 6.5 5.6

1.97 1.76 1.53 1.37 1.54 1.83 1.48 1.79

1.20 3.33 1.17 3.67 1.00 2.00 1.67 2.67

V (SE) T (SE) V × T (SE) BB DSD EC GA Rs Sg

*** (0.44) *** (0.31) ** (0.62) 5.6 7.1 8.6 7.1 8.7 5.5

*** (17.08) ** (12.36) ** (21.35) 287.2 226.6 241.5 231.3 256.1 236.6

DSD EC GA

2011

treatment Rs Sg Rs Sg Rs Sg Rs Sg

DSD EC GA

sign.

ab a bc e bc cd cd de

a bc c bc c b bc c

* (0.39) NS ** (0.49) 7.5 5.7 6.3 6.1 6.4 6.3

a bc bc d bc ab b a

*** (0.05) NS *** (0.08) 1.8 1.5 1.7 1.6 1.6 1.7

*** (0.12) *** (0.17) NS 2.3 ab 2.4 a 1.5 c 2.2 b 1.3 b 2.9 a

a

Different letters in rows denote significant differences in treatment (Duncan test, p < 0.05). bThe significance is designated by asterisks as follows: *statistically significant differences at P-value below 0.05; **statistically significant differences at P-value below 0.01; ***statistically significant differences at P-value below 0.001. cSE = standard error for significant term.

interaction was also significant (p = 0.01). The CIRG index ranged from 6.5 to 7.1 in 2010 and from 5.3 to 8.6 in 2011, which indicated a very dark-violet skin of the eggplant fruit. According to Carreño et al.,36 a CIRG index of 5 indicates reddark violet skin, 5.7 indicates red-black fruit skin, and higher than 6 indicates blue-black fruit skin. In 2010, the darkest fruit skin was recorded with variety EC, with a CIRG index of 7.0, while the CIRG indexes of other varieties were lower than 6.9. In 2011, grafting significantly increased the darkness of the fruit peel with indexes for BB from 6.5 (self-grafted plants) to 8.6 (plants grafted onto BE), while with EC darkness decreased from 7.1 (self-grafted plants) to 5.5 (plants grafted onto BE). The length/width ratio of fruit was significantly influenced by variety (p = 0.001) in 2010. Although ANOVA did not confirm a significant effect of grafting on fruit shape in 2010, we found more elongated shapes with self-grafted plants of all varieties, with a higher length/width ratio compared to fruits from plants grafted onto rootstock. A significant effect of varieties on fruit

shape was expected, since fruit shape is highly genetically controlled.37 EC had the most elongated fruits among all tested varieties. In 2011, the significant impact of the V × T interaction (p = 0.001) indicated that fruits of BB and landrace DSD plants grafted onto BE were more elongated than the fruits of self-grafted plants; with EC and GA, the opposite effect was recorded. Finally, an important visible trait of eggplant fruit is calyx prickles, which is an undesirable trait for handling eggplant fruits. In both years, ANOVA confirmed the significant impact of grafting on decreasing the amount of calyx prickles, since the scores of this trait for fruits from grafted plants were lower than those from self-grafted plants. A significant effect of variety on calyx prickles was reflected in the highest scores for it in fruits from landrace DSD, in both years, compared to those of other commercial varieties. The lightness of the fruit pulp immediately after cutting (L0) was similar in grafted and self-grafted plants, with values 10507



10508

NS NS NS

* (0.02) ** (0.12)

a a b b 2.8 2.9 2.1 2.2 4.2 5.8 5.4 4.5

NS

b a ab b

NS

2.2 3.7 3.3 3.5

NS NS

** (0.05) * (0.86)

a a b b 2.1 2.1 1.8 1.9 77.8 80.4 79.2 80.6

NS

b a ab a

NS

1.9 2.9 80.6 81.2

NS NS

* (0.78) * (0.22)

ab a ab a 78.9 80.9 79.3 80.2 8.3 5.8 7.2 6.3

NS

a b ab b

NS

80.8 81.6 7.6 8.2

NS NS

* (0.38) ** (0.19)

3.9 a 3.9 a 2.8 b 3.3ab b a b b

NS ** (0.22)d

4.8 3.7 3.4 3.5

2.0 2.7 2.8 b 4.8 a

NS NS

** (0.216) NS

b a ab a 1.6 2.4 2.2 2.8 78.6 80.4 79.2 80.6

NS NS

1.4 1.9 80.4 80.9

NS

NS

sign.

V×T

78.2 80.7 79.3 80.2 V

BB DSD EC GA

NSc sign.b

81.8 80.9 Rs Sg

a

T

Different letters in rows denote significant differences in treatment (Duncan test. p < 0.05). bThe significance is designated by asterisks as follows: *statistically significant differences at P-value below 0.05; **statistically significant differences at P-value below 0.01; ***statistically significant differences at P-value below 0.001. cNS = not significant. dStandard errors are in the parentheses.

** (0.31)

b a b a 6.8 8.6 7.2 8.2

NS

6.7 7.8

ΔL30 central lateral ΔL10 central

L0

lateral

central

ΔL10

lateral

central

ΔL30

lateral

central

L0

lateral

central

year 2011 year 2010

Table 4. Changes in Browing of Pulp Tissue Measured Rapidly after Cutting (L0) and Browning Potential (ΔL10 after 10 min, ΔL30 after 30 min) in Central and Lateral Sections of Eggplant As Affected by Grafting and Varietiesa

between 80 and 82.0 and with no significant impact of grafting in either the central or lateral parts of the pulp surface (Table 4). Differences were significant among varieties, in both years. DSD and GA showed whiter pulp, both laterally and centrally, while fruits from BB had the darkest pulp. The effect of grafting combination on the browning potential was assessed by measurements of the lightness of the fruit pulp 10 min (L10) and 30 min (L30) after slicing, and the difference with L0 was calculated as the index of browning potential.38 ANOVA showed a significant effect of rootstock (p = 0.01) on the browning potential only 10 min after cutting (L10) in 2010 and of varieties (p = 0.001) in both years. Browning was more evident in the peripheral part of the fruit section, both 10 and 30 min after cutting. In 2010, the effect of grafting on changes of browning pulp tissues was recorded in lower browning potential (ΔL10 was 2.8) on the lateral part of the pulp of grafted fruit compared to the fruits of self-grafted plants (ΔL10 was 4.8). After 30 min no significant differences regarding the grafting effect on browning potential were found, and the same effects were also recorded in 2011. In 2011 grafting did not affect the browning potential of eggplant pulp 10 and 30 min after cutting. In relation to varieties, a higher browning potential after 30 min was found in the lateral section of BB in 2010 and DSD and GA in 2011. The variety with the lowest browning potential in the lateral section after 30 min was DSD in 2010 and BB and EC in 2011. In the four eggplant varieties that were grafted onto BE tomato rootstock, we identified and quantified 13 phenolics (Tables 5−7) belonging to four groups: hydroxycinnamic acids, flavonols, flavanols, and anthocyanins. Compounds of the first three groups were identified in eggplant pulp, while anthocyanins were identified in the eggplant peel. Great differences in relation to variety and grafting treatment were found in the individual phenolic groups between the years. These results are in accordance with data reported by Lata et al.,39 who observed up to 70% differences in phenolics between seasons. In the fruit pulp we found the following hydroxycinnamic acids: chlorogenic, caffeic, p-coumaric, and ferulic acids. Hydroxycinnamic acids were the highest represented group of phenolics in the eggplant fruit of all four varieties, ranging from 25 to 45% in 2010 and from 34 to 51% in 2011. For total hydroxycinnamic acids, ANOVA showed a statistically significant effect of variety (p = 0.001) in 2010 and the interaction V × T in both years. In 2010, fruits of BB (from grafted and self-grafted plants) had the highest total hydroxycinnamic acid contentration, and no significant differences were found between them. The effect of grafting on hydroxycinnamic acid content was recorded with DSD, where grafting onto BE caused their increase in comparison with the fruits from self-grafted plants and with GA and EC, where the opposite effect was found. In 2011, grafting had no effect on changes in total hydroxycinnamic acid content in fruits of commercial varieties while for DSD a significant decrease was found (Tables 6 and 7). In terms of quantity, quercetins are a minor phenol group in eggplant fruits, ranging from 1 to 4% of the total analyzed phenolic concentration. The analysis of flavonols covered four types of quercetin glycoside: quercetin 3-rhamnoside accounted for approximately 75−90% of total flavonol concentration, followed by quercetin 3-rutinoside (4−17%), quercetin 3-glucoside (2−8%) and quercetin 3-galactoside (1−2%). Total flavonols were significantly influenced by variety and interaction of V × T in 2010 and by both main factors and their interaction in 2011. In 2010, grafting on rootstock significantly increased the total

lateral

Article



Article

Table 5. Identification of Phenolic Compounds in the Peel and Pulp of Eggplant Fruit in Negative and Positive Ions with HPLC−MS and MS2 phenolic group hydroxycinnamic acids

flavanols flavonols

anthocyanins

a

λmax (nm) 328, 241, 310, 295, 279, 279, 354, 356, 356, 353, 280, 279, 281,

234 323 225 322 234 234 234 256, 234 254, 234 268, 255 525 526 525

M+ or [M − H]−(m/z)a

MS2 (m/z)

tentative identification

353 179 163 193 289 289 609 463 463 447 611 773 773

191, 179 135, 161 119 134, 178, 149 245 245 301 301 301 301 465/303 611/465/303 611/465/303

chlorogenic acid caffeic acid p-coumaric acid ferulic acid catechin epicatechin quercetin 3-rutinoside quercetin 3-galactoside quercetin 3-glucoside quercetin 3-rhamnoside delphinidin 3-rutinoside delphinidin 3-rutinoside-5-galactoside delphinidin 3-rutinoside-5-glucoside

Anthocyanins were obtained in positive ion mode and other phenolics in negative ion mode.

flavonols in fruits of the landrace DSD and decreased in GA. A more consistent impact of grafting on total flavonol concentrations was observed in 2011, where grafting increased their concentration in fruits of EC and GA (Tables 6 and 7). Within flavanols, monomeric catechin and epicatechin were analyzed in eggplant pulp. Catechin was a more abundant individual flavanol in the eggplant fruits than epicatechin, representing 50−80% of the total flavanol concentration. Their concentrations ranged from 30 to 45% in 2010 and from 25 to 40% in 2011 of the total phenolic concentration. Significant changes in total flavanols were observed only in 2010, for which ANOVA showed a significant impact of variety and interaction V × T. Fruits of grafted EC and GA had significantly lower total flavanol concentrations than fruits from self-grafted plants. The opposite effect, with significantly higher total flavanol concentration was found in grafted fruits from DSD compared to self-grafted fruits. In terms of quantity, anthocyanins were the third most represented phenolic group in eggplant fruits after hydroxycinnamic acids and flavanols. Their concentration ranged from 15 to 30% of the total analyzed phenolic concentration. In the fruit peel we identified and quantified the following anthocyanins: delphinidin 3-rutinoside, delphinidin 3-rutinoside-5-galactoside, and delphinidin 3-rutinoside-5-glucoside. Delphinidin 3-rutinoside was found in the highest mean concentrations in all the samples and represented 90−95% in 2010 and 83−92% in 2011 of the total anthocyanin concentration. Delphinidin 3-rutinoside-5galactoside was the second most represented, ranging from 2 to 7% in 2010 and from 7 to 13% in 2011. Delphinidin 3-rutinoside5-glucoside was found in the lowest mean concentrations, ranging from 1 to 3% in both years. ANOVA confirmed a significant effect of grafting (p = 0.01) on total anthocyanin concentration only in 2010, when grafting decreased the total anthocyanin concentration in the peel of eggplant fruits with all tested varieties.

a scion/rootstock combination plays an important role in the achievement of the established tasks.5,7,10 It is well-known that scion variety mainly affects the final yield and quality traits of fruit in grafted plants,40 but rootstock effects can alter these characteristics,1,3,4 possibly due to changes in vigor and concentration of growth regulators induced by the rootstocks.8 Further, differences in the requirements for assimilating mineral nutrients between tomato (rootstock) and eggplant (scion) also altered the quality of fruit yield.41 In our study, higher yield and the changes of visual characteristics of fruits from grafted and self-grafted plants could be explained by the successful adoption by the scion of the main rootstock’s characteristics, already described in Table 1. The lower presence of calyx prickles, observed in fruits from grafted plants, may indicate more vigorous and balanced growth41 of grafted plants than selfgrafted ones, since the prickles in the eggplant calyx are probably caused by biotic or abiotic stresses.17 Eggplant has a high antioxidant capacity, mainly attributed to its high content of phenolic compounds.14 First evaluations of phenolic acid constituents in eggplant fruit from different accessions and varieties were reported by Stommel and Whitaker12 latter in phytochemical investigations, and the impact of different cultivation systems, grafting techniques, and methods of sample preparation on phenolic constituents were examined.3,8,28,42 In accordance with the above-mentioned studies, the analyzed composition, and the content of the main phenolic groups (hydroxycinnamic acids, flavonols, flavanols, and anthocyanins) in eggplant pulp and peel showed high dependence not only on variety but also on rootstock, as well as on environmental conditions, since the phenolic profile varied during the two growing periods. In 2010, less solar radiation and lower mean daily temperatures (Table 2) led to less favorable environmental conditions for growth and development of eggplant fruits. It seems that higher vigor of grafted plants of commercial varieties is more expressed under such temperate environmental conditions, where rootstock hastened plant growth and development, which resulted in higher yield. We picked a significantly higher number of fruits per plant (7.5−8) from plants of grafted commercial varieties compared to the grafted landrace (Table 3). On the other hand, it could be expected that fruits from grafted commercial varieties had not reached physiological maturity at harvesting, because they grew faster than selfgrafted plants and we picked them at a younger maturity stage. At physiological maturity, the contents of sugars, ascorbic acid,

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DISCUSSION In recent years, a high quality of vegetable fruits is even more important than total fruit yield, due to the benificial role of vegetables in the human diet.11 External quality described by visual traits such as fruit size, shape, color, and calyxs prickles are important criterion in making purchasing decisions of eggplant fruits.1 Among many strategies, such as genetic selection, optimization of the environmental conditions, and agricultural practices, grafting represents an efficient technological tool where 10509


10510

V

(21.4)

(19.3)c (2.7) (0.9)

** (0.21) NS *** (0.05) *** (1.48) *** (1.59) NS *** (11.29) *** (41.41) NS *** (1.17) *** (0.42) NS ** (46.83)

*** *** *** NS ***

T

NS NS NS NS NS NS *** (7.9) *** (29.1) *** (14.2) * (0.8) NS ** (15.0) NS

NSd NS **(0.7) NS NS

V×G

NS NS NS *** (2.1) *** (2.2) NS *** (16.0) *** (58.2) NS *** (1.6) NS NS ** (64.7)

*** (27.3) ***(3.6) *** (1.4) NS *** (30.3)

BB

0.97 b 0.28 0.49 a 19.6 21.3 270.0 153.1 424.2 181.2 14.7 5.9 a 201.9 789.4

389.4 31.1 3.5 3.5 427.6

DSD

0.64 b 0.28 0.14 b 16. 17.7 150.2 103.3 253.1 132.1 4.8 3.6 b 140.5 583.4

279.1 26.3 3.0c 4.1 312.5

V EC

1.61 a 0.32 0.13 b 14.8 16.9 235.6 139.1 375.6 194.1 9.6 2.7 b 206.3 631.9

213.7 27.3 12.5 3.7 257.3

GA

1.85 a 0.45 0.45 a 24.6 27.4 224.1 49.3 274.1 163.8 7.0 2.6 b 173.5 565.8

262.7 12.9 6.9 3.7 286.8

Sg

1.11 0.33 0.35 21.8 23.7 187.4 147.1 400.2 201.5 a 10.5 3.9 215.9 a 666.5

297.1 26.1 8.7 4.2 336.3

T Rs

1.43 0.31 0.26 16.0 18.5 253.4 76.1 263.2 134.1 b 7.5 3.5 145.2 b 618.8

275.4 22.8 4.2 3.3 305.8

BB × Sg

0.7 0.3 0.5 20.1 b 21.7 b 260.1 159.0 ab 419.2 ab 187.6 15.9 b 6.4 210.0 1178.2 b

480.9 a 38.5 ab 3.1 bcd 4.6 527.2 a

BB × Rs

1.2 0.2 0.5 19.1 bc 20.9 b 280.8 148.6 b 429.4 a 174.8 13.6 ab 5.5 193.9 1098.6 ab

413.0 ab 36.0 b 3.3 bc 2.1 454.4 a 0.5 0.2 0.1 14.7 d 15.7 d 136.5 81.8 cd 218.3 c 162.1 0.9 f 2.9 165.9 540.1 bc

169.4 de 19.8 c 2.2 d 3.6 231.5 ef

DSD × Sg

0.8 0.3 0.2 22.4 b 23.7 b 175.9 160.2 ab 336.1 abc 102.3 8.6 de 4.2 115.1 868.8 e

348.5 bc 38.8 ab 5.3 bc 0.8 393.4 bc

DSD × Rs

V×T

1.1 0.2 0.1 16.4 bc 17.8 bc 288.1 195.8 a 483.9 a 236.2 14.5 ab 3.3 254.0 1038.0 a

215.5 d 47.5 a 15.7 a 3.6 282.3 de

EC × Sg

2.1 0.4 0.1 13.3 cd 15.9 d 183.5 83.8 c 267.3 bc 151.9 4.6 ef 2.0 158.6 590.6 cd

120.9 e 20.3 c 5.4 b 2.1 148.8 f

EC × Rs

1.8 0.5 0.6 28.5 a 31.3 a 288.9 72.9 c 361.9 ab 220.2 10.7 f 2.8 233.7 973.2 bc

307.4 c 17.7 c 15.7 a 5.6 346.4 cd

GA × Sg

GA × Rs

1.9 0.5 0.3 20.8 b 23.5 b 160.2 26.1 d 186.3 c 107.5 3.4 bc 2.4 113.2 516.3 de

184.1 de 6.3 d 1.4 cd 1.6 193.3 ef

a Different letters in rows denote significant differences in treatment (Duncan test, p < 0.05). bSe = standard error for the significant term. cThe significance is designated by asterisks as follows: *statistically significant differences at P-value below 0.05; **statistically significant differences at P-value below 0.01; ***statistically significant differences at P-value below 0.001. dNS = not significant.

chlorogenic acid caffeic acid p-coumaric acid ferulic acid tot. hydroxycinnamic acids q 3-rut q 3-gal q 3-gluc q 3-rham tot. flavonol catechin epicatechin tot. flavanol del 3-rut del 3-rut-5-gal del 3-rut-5-glu tot. anthocianins tot. phenolics

significance (SE)b

Table 6. Significance for Varieties (V), Treatment (T), and Interaction (V × T), with Standard Error in Parentheses; Means of Individual Phenolic Compounds (in mg kg−1 FW); and Results of Duncan’s Multiple Comparison Test for Significant Terms, for the Year 2010a

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10511

BB 326.6 24.8 3.7 b 3.8 b 359.0 1.6 0.2 0.8 16.5 19.8 151.4 b 102.8 253.7 167.2 20.9 a 5.2 a 193.4 632.0

V×G ** (27.2)e * (4.7) NS NS ** (31.1) * (0.5) ** (0.1) ** (0.2) * (2.5) * (2.7) NS * (19.6) NS NS NS NS NS ** (68.8)

T

NSd NS * (1.2) NS NS

NS NS ** (0.1) ** (1.3) * (1.4) NS NS NS NS NS NS NS NS

NS NS NS ** (1.7) * (1.9) * (24.2) NS NS NS ** (2.0) ** (0.5) NS NS

V

NS NS ** (1.6) * (0.7) NS

DSD

1.3 0.3 0.8 17.8 20.4 155.3 b 95.1 250. 5 128.4 18.9 a 4.4 a 151.8 602.7

299.2 23.0 2.8 b 6.7 a 331.8

V EC

1.8 0.2 0.7 9.6 12.4 258.4 85.9 344.8 171.2 17.3 a 4.6 a 193.2 655.9

259.2 20.8 14.4 a 4.6 b 299.1

GA

0.8 0.3 0.5 16.4 18.1 181.31 57.0 238.3 138.0 10.6 b 2.6 b 151.3 560.2

279.7 13.8 5.3 b 4.7 ab 303.7

Sg

1.3 0.3 0.9 12.4 15.1 178.5 87.2 256.7 138.5 15.0 3.7 157.3 616.2

300.7 21.1 8.5 a 4.9 335.3

Tc Rs

1.4 0.2 0.5 17.7 19.9 194.7 82.9 277.7 164.0 18.8 4.6 187.6 609.1

281.7 20.1 4.6 b 5.03 311.4

BB × Sg

2.2 ab 0.3 bc 1.5 a 13.4 bcd 17.4 abc 110.1 76.7 abc 186.8 137.9 19.6 4.8 162.3 747.9 bcd

353.6 ab 18.6 abc 6.0 3.4 381.5 ab

BB × Rs

1.0 bc 0.2 bc 0.3 c 19.6 ab 21.2 ab 192.8 127.9 a 320.7 196.7 22.2 5.7 224.5 903.0 a

299.8 abc 31.0 a 1.6 4.2 336.6 abc 1.4 bc 0.6 a 1.0 ab 19.4 abc 22.4 ab 158.3 121.8 ab 280.2 111.6 14.3 3.1 129.0 842.7 ab

372.4 a 29.5 ab 2.7 6.6 411.2 a

DSD × Sg

1.3 bc 0.2 bc 0.7 bc 16.3 abcd 18.5 abcd 152.3 68.4 cd 220.7 145.4 23.6 5.7 174.7 666.5 cde

226.1 c 16.6 bcd 3.0 6.9 252.5 d

DSD × Rs

V×T EC × Sg

0.9 c 0.1 c 0.7 bc 6.9 e 8.6 e 237.8 113.1 abc 351.0 185.4 16.8 4.4 206.6 853.9 ab

238.3 c 27.4 abc 17.3 4.7 287.7 cd

EC × Rs

2.8 a 0.4 a 0.8 b 12.3 c 16.2 abc 279.0 58.8 c 337.8 157.1 17.9 4.9 179.9 844.4 a

280.3 b 14.3 c 11.5 4.5 310.5 b

0.9 b 0.3 b 0.7 b 10.2 d 12.2 de 207.9 37.2 d 245.1 119.1 9.4 2.8 131.4 649.8 c

238.8 c 9.0 d 8.3 5.0 261.1c

GA × Sg

GA × Rs

0.8 c 0.3 bc 0.4 c 22.6 a 24.2 a 154.7 76.9 abcd 231.6 156.9 11.9 2.5 171.2 773.3 bc

320.8 ab 18.6 abcd 2.3 4.5 346.3 abc

a Different letters in rows denote significant differences in treatment (Duncan test, p < 0.05). bSE = standard error for significant term. cSg = self-grafted. Rs = rootstock. dNS = not significant. eThe significance is designated by asterisks as follows: *statistically significant differences at P-value below 0.05; **statistically significant differences at P-value below 0.01; ***statistically significant differences at P-value below 0.001.

chlorogenic acid caffeic acid p-coumaric acid ferulic acid tot. hydroxycinnamic acids q 3-rut q 3-gal q 3-gluc q 3-rham tot. flavonol catechin epicatechin tot. flavanol del 3-rut del 3-rut-5-gal del 3-rut-5-glu tot. anthocianins tot. phenolics

significance (SE)b

Table 7. Significance for Varieties (V), Treatment (T), and Interaction (V × T), with Standard Error in Parentheses; Means of Individual Phenolic Compounds (in mg kg−1 FW); and Results of Duncan’s Multiple Comparison Test for Significant Terms, for the Year 2011a

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Article

be explain with findings reported by Hanson,2 who suggest that environmental factors, above all light, temperature and water management, influenced the types or levels of phenolic compounds in eggplant fruits. During the growing seasons in our study, weather conditions were very similar, with temperatures slightly above the long-term average in both years, but with a little lower solar radiation in 2010 than in 2011, which contributed to less suitable growing conditions for eggplants in that year. In accordance with the studies on the impact of different factors on browning potential of eggplant fruit pulp,17,18,33 the browning potential in our study showed high dependence on variety and partly on grafting combination. As regards the different correlations between phenolic contents and browning potential (positive for EC and GA and negative for the landrace DSD), the importance of other main antioxidants, such as reduced ascorbate, could be evidenced.18,38 The content of ascorbic acid, which has antibrowning properties because it reduces enzymatically formed o-quinones to their precursor diphenols, is also genetically, developmentally, and environmentally dependent;17 therefore, variations of its content in fruits from our treatments could be expected. The syntheses of sugars, ascorbic acid, and polyphenols are developmentally conditioned and reached their maximum values about 6 weeks from eggplant fruit set. This fact emphasizes the importance of considering this point for determination of the physiological maturation stage of the fruit,48 in order to harvest eggplant fruits with higher nutritional value. There are also some other variety-dependent factors, like intracellular pH, which affects the activity of the polyphenol oxidase enzyme, or cellular factors, such as cell size, which may have a role in browning and color evaluation of the fruit pulp.25 In conclusion, the impact of grafting commercial eggplant varieties and landrace onto tomato rootstock on internal and external eggplant fruit characteristics is not equal and is largely conditioned by scion/rootstock combination and environmental conditions. For all tested varieties data indicated a positive effect of grafting on yield and visual traits of eggplant fruits. Grafted plants were more vigorous than self-grafted plants and gave higher yield. For some varieties grafting influenced also fruit shape and size and for all varieties decreased the presence of calyx prickles. Higher vigor of grafted plants negatively influenced the concentration of anthocyanins; therefore, pruning of grafted plants to improve the color and phenolics concentration in eggplants peel should be performed during the growing period. For some of the commercial varieties grafted onto tomato rootstock, a decrease of the phenolic content in eggplant pulp was found, compared to self-grafted plants. The effect of grafting eggplant landrace onto tomato rootstock showed an inconsistent trend in the phenolics content of eggplant samples, which indicated that the synthesis of phenolics in landrace fruit is probably dependent also on environmental factors, especially on light conditions. With additional analysis with which a higher presence of reducing antioxidants in eggplant fruits could be confirmed, our results would become more promising and useful, especially when grafted varieties showed better characteristics and as such deserve more attention by rootstock breeders. Further research work should focus on the evaluation of the complete chemical profile of eggplant fruits picked from the different scion/roostock combinations and on the observation of their growth and development. With this knowledge, appropriate criteria for the determination of the physiological maturity stage of fruits can be define in order to get

and polyphenols are the highest in eggplant fruits and then significantly decreased.48 Our assumption was partly confirmed by the chemical analysis of phenolic constituents in eggplant fruits, which showed a lower concentrations of all phenolic constituents in grafted fruits in comparison with the fruits from self-grafted plants. The opposite effect was found for the landrace/rootstock combination, where we harvested only five fruits per plant in that year, which indicates that fruits from the landrace grew more slowly; thus, they could reach their physiological maturity by harvest date, which was confirmed also with an increase of the phenolic contents in grafted plants compared to self-grafted ones. Anthocyanins are the most important group within flavonoids for the production of a dark red or purple color of the eggplant peel.21 The composition of anthocyanins in fruits from our study was relatively similar to those observed by Sadilova et al.21 and Wu and Prior.43 On the other hand, the composition of anthocyanins is largely conditioned by eggplant variety and growth conditions.2,23,38,44 This could be one of the reasons why our results differed from the data reported by Azuma et al.,45 who identified an acylated anthocyanin, known as nasunin, as the prevailing anthocyanin in Japanese eggplant varieties. In our study, the concentrations of anthocyanins, which were analyzed in eggplant peel in 2010, showed high dependence on grafting. Their concentration significantly decreased in fruits from grafted plants compared to the fruits from self-grafted plants. This response was probably a consequence of more shaded fruits, since grafted plants had a higher habitus with much bigger leaves (data not shown), with which the fruits were covered. Since accumulation of anthocyanins is strongly light-exposure-dependent,29,46 it could be additionally suggested that, in order to produce fruits with a higher anthocyanin concentration and thus with higher nutritional value, grafted eggplant plants should properly be pruned and illuminated. As eggplant is ranked among the top 10 vegetables in terms of antioxidant activity, mainly due to the fruit phenolic constituents, the high browning potential of the fruit pulp could be expected.1,28,18 Browning appears on cutting, when disruption of cellular structures leads to release of the enzyme polyphenol oxidase (PPO), which oxidizes phenolics, and in the presence of oxygen, o-quinones are polymerized, causing browncolored pigments.18 Eggplant varieties differed in their extents of postcut browning, which could be due to variations in the PPO activity or level of soluble phenolics.7,17,18 In contrast to the findings of Gisbert et al.8 and Moncada et al.,3 who reported that little or no effect of grafting on fruit phenolics content was found, in our study grafting decreased the phenolics concentration in fruits of commercial varieties in 2010, while the landrace/rootstock combination gave a significant increase (in 2010) and decrease (in 2011) of phenolics concentration. Higher phenolic concentration in grafted DSD eggplant pulp in 2010, in addition to the lowest fruit yield among the grafted treatments (Table 3), may be an additional indicator of the stress in this scion/rootstock combination, since stress conditions induce an accumulation of phenolics.1,47 An inverse effect of grafting in DSD in the next year of the study probably indicated a higher diversity among landrace plants compared to the plants of the other commercial hybrid varieties, for which a very similar pattern of phenolic concentration changes were observed in both years. An interesting result of our study is that the fruits from the same landrace/rootstock grafted combination behaved differently during the two growing season, which could 10512



Article

Solanum melongena inhibits PAR2 agonist-induced inflammation. Clin. Chim. Acta 2003, 328, 39−44. (17) Prohens, J.; Rodriguez-Burruezo, A.; Raigon, M. D.; Nuez, F. Total phenolic concentration and browning susceptibility in a collection of different varietal types and hybrids of eggplant: Implications for breeding for higher nutritional quality and reduced browning. J. Am. Soc. Hortic. Sci. 2007, 132, 638−646. (18) Mishra, B. B.; Gautam, S.; Sharma, A. Free phenolics and polyphenol oxidase (PPO): The factors affecting post-cut browning in eggplant (Solanum melongena). Food Chem. 2013, 139, 105−114. (19) Huang, H. Y.; Chang, C. K.; Tso, T. K.; Huang, J. J.; Chang, W. W.; Tsai, Y. C. Antioxidant activities of various fruits and vegetables produced in Taiwan. Int. J. Food Sci. Nutr. 2004, 55, 423−429. (20) Ichiyanagi, T.; Kashiwada, Y.; Shida, Y.; Ikeshiro, Y.; Kaneyuki, T.; Konishi, T. Nasunin from eggplant consists of cis−trans isomers of delphinidin 3-[4-(p-coumaroyl)-L-rhamnosyl (1→6)glucopyranoside]5-glucopyranoside. J. Agric. Food Chem. 2005, 53, 9472−9477. (21) Sadilova, E.; Stintzing, F. C.; Carle, R. Anthocyanins, colour and antioxidant properties of eggplant (Solanum melongena L.) and violet pepper (Capsicum annuum L.) peel extracts. Z. Naturforsch. C 2006, 61, 527−535. (22) Okmen, B.; Sigva, H. O.; Mutlu, S.; Doganlar, S.; Yemenicioglu, A.; Frary, A. Total antioxidant activity and total phenolic contents in different turkish eggplant (Solanum melongena L.) cultivars. Int. J. Food Prop. 2009, 12, 616−624. (23) Raigon, M. D.; Prohens, J.; Munoz-Falcon, J. E.; Nuez, F. Comparison of eggplant landraces and commercial varieties for fruit content of phenolics, minerals, dry matter and protein. J. Food Compos. Anal. 2008, 21, 370−376. (24) Savvas, D.; Lenz, F. Influence of NaCl concentration in the nutrient solution on mineral composition of eggplants grown in sand culture. J. Appl. Bot. 1996, 70, 124−127. (25) Concellon, A.; Anon, M. C.; Chaves, A. R. Characterization and changes in polyphenol oxidase from eggplant fruit (Solanum melongena L.) during storage at low temperature. Food Chem. 2004, 88, 17−24. (26) Raigon, M. D.; Rodriguez-Burruezo, A.; Prohens, J. Effects of organic and conventional cultivation methods on composition of eggplant fruits. J. Agric. Food Chem. 2010, 58, 6833−6840. (27) Luthria, D.; Singh, A. P.; Wilson, T.; Vorsa, N.; Banuelos, G. S.; Vinyard, B. T. Influence of conventional and organic agricultural practices on the phenolic content in eggplant pulp: Plant-to-plant variation. Food Chem. 2010, 121, 406−411. (28) Singh, A. P.; Luthria, D.; Wilson, T.; Vorsa, N.; Singh, V.; Banuelos, G. S.; Pasakdee, S. Polyphenols content and antioxidant capacity of eggplant pulp. Food Chem. 2009, 114, 955−961. (29) Manach, C.; Scalbert, A.; Morand, C.; Remesy, C.; Jimenez, L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727−747. (30) Lee, J. M. Cultivation of grafted vegetables. 1. Current status, grafting methods, and benefits. HortScience 1994, 29, 235−239. (31) Fernandez-Lopez, J. A.; Almela, L.; Munoz, J. A.; Hidalgo, V.; Carreno, J. Dependence between colour and individual anthocyanin content in ripening grapes. Food Res. Int. 1998, 31, 667−672. (32) Larrigaudiere, C.; Lentheric, I.; Vendrell, M. Relationship between enzymatic browning and internal disorders in controlledatmosphere stored pears. J. Sci. Food Agric. 1998, 78, 232−236. (33) Concellon, A.; Anon, M. C.; Chaves, A. R. Effect of low temperature storage on physical and physiological characteristics of eggplant fruit (Solanum melongena L.). Lebensm.-Wiss. Technol. 2007, 40, 389−396. (34) Mikulic-Petkovsek, M.; Slatnar, A.; Stampar, F.; Veberic, R. The influence of organic/integrated production on the content of phenolic compounds in apple leaves and fruits in four different varieties over a 2-year period. J. Sci. Food Agric. 2010, 90, 2366−2378. (35) Marks, S. C.; Mullen, W.; Crozier, A. Flavonoid and chlorogenic acid profiles of English cider apples. J. Sci. Food Agric. 2007, 87, 719− 728.

the eggplant with higher content of substances responsible for flavor, nutritional value, and sensorial characteristics of eggplant fruits.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Fax: +386 1 423 10 88. Tel: +386 1 320 31 13. Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED BB, Blackbell; DSD, Domači srednje dolgi; EC, Epic; GA, Galine; BE, Beaufort; V, variety (commercial varieties and landrace); T, treatment (self-grafted plants and plants grafted onto rootstock); Rs, rootstock; Sg, self-grafted plants; sign., significance.

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REFERENCES

(1) Gisbert, C.; Prohens, J.; Nuez, F. Performance of eggplant grafted onto cultivated, wild, and hybrid materials of eggplant and tomato. Int. J. Plant Prod. 2011, 5, 367−380. (2) Hanson, P. M.; Yang, R. Y.; Tsou, S. C. S.; Ledesma, D.; Engle, L.; Lee, T. C. Diversity in eggplant (Solanum melongena) for superoxide scavenging activity, total phenolics, and ascorbic acid. J. Food Compos. Anal. 2006, 19, 594−600. (3) Moncada, A.; Miceli, A.; Vetrano, F.; Mineo, V.; Planeta, D.; D’Anna, F. Effect of grafting on yield and quality of eggplant (Solanum melongena L.). Sci. Hortic. 2013, 149, 108−114. (4) Passam, H. C.; Stylianou, M.; Kotsiras, A. Performance of eggplant grafted on tomato and eggplant rootstocks. Eur. J. Hortic. Sci. 2005, 70, 130−134. (5) Lee, J. M.; Oda, M., Grafting of herbaceous vegetable and ornamental crops. Hortic. Rev. 2003, 28. (6) Bletsos, F.; Thanassoulopoulos, C.; Roupakias, D. Effect of grafting on growth, yield, and Verticillium wilt of eggplant. HortScience 2003, 38, 183−186. (7) King, S. R.; Davis, A. R.; Zhang, X. P.; Crosby, K. Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Sci. Hortic. 2010, 127, 106−111. (8) Gisbert, C.; Prohens, J.; Raigon, M. D.; Stommel, J. R.; Nuez, F. Eggplant relatives as sources of variation for developing new rootstocks: Effects of grafting on eggplant yield and fruit apparent quality and composition. Sci. Hortic. 2011, 128, 14−22. (9) Schwarz, D.; Rouphael, Y.; Colla, G.; Venema, J. H. Grafting as a tool to improve tolerance of vegetables to abiotic stresses: Thermal stress, water stress and organic pollutants. Sci. Hortic. 2010, 127, 162− 171. (10) Davis, A. R.; Perkins-Veazie, P.; Hassell, R.; Levi, A.; King, S. R.; Zhang, X. P. Grafting effects on vegetable quality. HortScience 2008, 43, 1670−1672. (11) Rouphael, Y.; Schwarz, D.; Krumbein, A.; Colla, G. Impact of grafting on product quality of fruit vegetables. Sci. Hortic. 2010, 127, 172−179. (12) Stommell, J. R.; Whitaker, B. D. Phenolic acid content and composition of eggplant fruit in a germplasm core subset. J. Am. Soc. Hortic. Sci. 2003, 128, 704−710. (13) Akanitapichat, P.; Phraibung, K.; Nuchklang, K.; Prompitakkul, S. Antioxidant and hepatoprotective activities of five eggplant varieties. Food Chem. Toxicol. 2010, 48, 3017−3021. (14) Cao, G. H.; Sofic, E.; Prior, R. L. Antioxidant capacity of tea and common vegetables. J. Agric. Food Chem. 1996, 44, 3426−3431. (15) Matsubara, K.; Kaneyuki, T.; Miyake, T.; Mori, M. Antiangiogenic activity of nasunin, an antioxidant anthocyanin, in eggplant peels. J. Agric. Food Chem. 2005, 53, 6272−6275. (16) Han, S. W.; Tae, J.; Kim, J. A.; Kim, D. K.; Seo, G. S.; Yun, K. J.; Choi, S. C.; Kim, T. H.; Nah, Y. H.; Lee, Y. M. The aqueous extract of 10513



Article

(36) Carreño, J.; Martínez, A.; Almela, L.; Fernández-López, A. Proposal of a index for the objective evaluation of the color of red table grapes. Food Res. Int. 1995, 28, 5. (37) Chen, N. C.; Li, H. M. Cultivation and breeding of eggplant. AVRDC, Shanuan, Tainan, Taiwan 2003, 1, 6. (38) Prohens, J.; Blanca, J. M.; Nuez, F. Morphological and molecular variation in a collection of eggplants from a secondary center of diversity: Implications for conservation and breeding. J. Am. Soc. Hortic. Sci. 2005, 130, 54−63. (39) Lata, B.; Przeradzka, M.; Binkowska, M. Great differences in antioxidant properties exist between 56 apple cultivars and vegetation seasons. J. Agric. Food Chem. 2005, 53, 8970−8978. (40) Munoz-Falcon, J. E.; Prohens, J.; Rodriguez-Burruezo, A.; Nuez, F. Potential of local varieties and their hybrids for the improvement of eggplant production in the open field and greenhouse cultivation. Int. J. Food Agric Environ. 2008, 6, 83−88. (41) Kawaguchi, M.; Taji, A.; Backhouse, D.; Oda, M. Anatomy and physiology of graft incompatibility in solanaceous plants. J. Hortic. Sci. Biotechnol. 2008, 83, 581−588. (42) Luthria, D. L.; Mukhopadhyay, S. Influence of sample preparation on assay of phenolic acids from eggplant. J. Agric. Food Chem. 2006, 54, 41−47. (43) Wu, X. L.; Prior, R. L. Identification and characterization of anthocyanins by high-performance liquid chromatography−electrospray ionization-tandem mass spectrometry in common foods in the United States: Vegetables, nuts, and grains. J. Agric. Food Chem. 2005, 53, 3101−3113. (44) Whitaker, B. D.; Stommel, J. R. Distribution of hydroxycinnamic acid conjugates in fruit of commercial eggplant (Solanum melongena L.) cultivars. J. Agric. Food Chem. 2003, 51, 3448−3454. (45) Azuma, K.; Ohyama, A.; Ippoushi, K.; Ichiyanagi, T.; Takeuchi, A.; Saito, T.; Fukuoka, H. Structures and antioxidant activity of anthocyanins in many accessions of eggplant and its related species. J. Agric. Food Chem. 2008, 56, 10154−10159. (46) Awad, M. A.; de Jager, A.; van der Plas, L. H. W.; van der Krol, A. R. Flavonoid and chlorogenic acid changes in skin of ‘Elstar’ and ‘Jonagold’ apples during development and ripening. Sci. Hortic. 2001, 90, 69−83. (47) Dixon, R. A.; Paiva, N. L. Stress-induced phenylpropanoid metabolism. Plant Cell 1995, 7, 1085−1097. (48) Esteban, R. M.; Molla, E. M.; Robredo, L. M.; Lopezandreu, F. J. Changes in the chemical-composition of eggplant fruits during development and ripening. J. Agric. Food Chem. 1992, 40, 998−1000.

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Grafting Influences Phenolic Profile and Carpometric Traits of Fruits of

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