Increased Temperature Produces Changes in the Bioactive

Feb 23, 2015 - However, there is limited information about the influence of high temperature on tomato composition when the stress is applied at diffe...
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Increased Temperature Produces Changes in the Bioactive Composition of Tomato, Depending on Its Developmental Stage Virginia Hernández, Pilar Hellín, Jose Fenoll, and Pilar Flores* Murcia Institute of Agri-Food Research and Development (IMIDA), c/Mayor s/n, La Alberca, Murcia, Spain ABSTRACT: The present study examines the effect of an increased day temperature on vitamin C and carotenoid concentrations in tomato, depending on the developmental stage of fruits when the stress is imposed. Plants were cultivated in a growth chamber initially at 24 °C, and the day temperature was increased to 32 °C when fruits belonging to six different fruit development stages could be differentiated. Vitamin C, phytoene, phytofluene, lycopene, γ-carotene, and violaxantin concentrations were significantly lower when a temperature of 32 °C was imposed during the advanced stages of fruit development compared to the levels observed in the control treatment. However, no effect or increased concentrations were observed when the temperature was increased in earlier stages, indicating the adaptation of the plant metabolism to high temperature. Finally, no effect on β-carotene concentration was observed, regardless of the fruit developmental stage when the temperature increase was applied. KEYWORDS: high temperature, climate warming, bioactive, ascorbic, HPLC

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temperatures expected as a result of global warming.9 The present study examines the duration and timing of increased day temperature on the vitamin C and carotenoid concentrations and fruit physical parameters in tomato.

INTRODUCTION Tomato (Solanum lycopersicum L.) is considered a potent source of vitamins and bioactive compounds.1 In particular, tomato fruit is considered as a valuable source of vitamin C and carotenoids. In higher plants, vitamin C is directly involved in multiple physiological essential processes, among many others the removal of active oxygen species, growth control, cell metabolism, cell division, expansion of the cell walls, and the synthesis of other metabolites.2 In addition, tomato is rich in carotenoids, especially lycopene and β-carotene, the main pigments responsible for the characteristic red color and potent antioxidants that reduce the risk of several human diseases.3,4 Furthermore, the tomato is a major source of other carotenoids, including lutein, which plays a fundamental role in the protection of vision,5 and others less studied such as phytoene and phytofluene, to which are attributed an inhibitory role in the progression of atherosclerosis.6 High temperature stress is associated with major losses in yield and the nutritional quality of fruits and vegetables. In tomato, an increase in air temperature has been shown to cause flower abortion and limit fruit set.7 As regards nutritional quality, Gautier et al.8 showed that increased temperature modified secondary metabolites to a greater extent than primary metabolites. According to these authors, raising the temperature up to 32 °C increased specific phenolic compounds but reduced the concentrations of ascorbate and several carotenoids in tomato. The effect of high temperature on secondary metabolite accumulation depended on the fruit development stage and also on the period of exposure to the temperature stress. However, there is limited information about the influence of high temperature on tomato composition when the stress is applied at different development stages in vineripened fruits. This information is very valuable taking into account the impact of high temperature stress on tomato yield and quality in crops grown in warm zones, especially under greenhouse conditions, as well as the increases in maximum © 2015 American Chemical Society

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MATERIALS AND METHODS

Tomato plants (Solanum lycopersicum cv. Velasco) were cultivated under growth chamber conditions in 15 L pots filled with a mix of coconut fiber and perlite (85:15), irrigated to drainage with Hoagland nutrient solution containing 14 N, 6 K, 4 Ca, 2 P, 1 S, and 1 Mg (mM) and 50 Cl, 25 B, 2 Mn, 2 Zn, 0.5 Cu, 0.5 Mo, and 20 Fe (μm). A 16/8 h day/night photoperiod was applied with a photon flux of about 550 μmol m−2 s−1 PAR. Air relative humidity was maintained around 70%. Plants were initially grown at 24 °C/13 °C (day/night temperature). Pollination was improved by hand-pollination (shaking the flowers), and plants were pruned by removing suckers. Fifty-one days after transplant, when fruits belonging to six different fruit development stages could be differentiated (trusses 3 through 5 for stages 2−6 and at the truss 6 for fruits at stage 1), the day temperature was increased to 32 °C (Table 1). Fruits belonging to each developmental stage were labeled on ten plants per treatment, using different plants for each developmental stage. Another group of plants was kept at 24 °C until the end of the experiment and was considered the control treatment. In the control plants, fruit from different trusses (3−6) were also selected. The trusses 1 and 2 were harvested in all the plants before increasing the temperature but not again until sampling to avoid modifying the fruit load. Fruits from the control treatment and those from the six increased temperature treatments (32 °C imposed to the six different development stages) were all sampled at the full-red stage of ripening, which corresponded to about 0, 6, 16, 22, 27, 36, and 44 days at high temperature (DHT), respectively. After turning, selected tomatoes were checked daily and sampled immediately when they showed a homogeneous red color to avoid over-ripening. Fruits with some appreciable damage or green or yellow parts were discarded. Six Received: Revised: Accepted: Published: 2378

November 14, 2014 February 20, 2015 February 23, 2015 February 23, 2015 DOI: 10.1021/jf505507h J. Agric. Food Chem. 2015, 63, 2378−2382

Article

Journal of Agricultural and Food Chemistry

reported in the literature. The major compounds were identified using commercially available external standards of carotenoids (DHI LAB, Hoersholm, Denmark), except for phytoene and phytofluene, which were expressed as β-carotene equivalents. The results were statistically analyzed using IBM SPSS Statistic 21 by analysis of variance (ANOVA) and Tukey’s test for differences between means.

Table 1. Stages of Development of Tomato Fruits Exposed for Different Number of Days to High Temperature (DHT) stage of development

description

DHTa

1 2 3 4 5 6

flowering diamb ≤ 30 mm diam ≤ 40 mm diam ≤ 50 mm diam ≤ 60 mm green fruit fully developed

44 36 27 22 16 6

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RESULTS AND DISCUSSION Fruit mean weight and equatorial and longitudinal diameter decreased as a result of the increased temperature (32 °C) (Table 2). These weight and size losses were proportional to the period of exposure to the stress, except in the case of fruits exposed to high temperature from flowering (stage 1), which showed fruit weights and sizes similar to those of the control fruits. The results obtained at this first stage could have been due to the higher incidence of flower abortion as a feedback controlling mechanism to prevent an excessive sink/source ratio.12 The reproductive process has previously been shown to be more sensitive to high temperature stress than vegetative growth. In addition, even within the different development stages of a fruit, certain stages are more sensitive. Thus, high temperature stress increased the tendency for younger flowers to abort due to shrunken pollen grain, failure of anther dehiscence, and an irregularly arranged endothecium and epidermis.13 Therefore, the higher incidence of flower abortion caused by high temperatures would only affect trusses in development stage 1 (truss 6), leading to an increase in the mean weight of the remaining fruits, and thus compensating the weight loss resulting from temperature stress. In addition, the increased total soluble content in fruit from the stage 1 treatment (Table 2) could be explained as a concentration effect due to a decreased sink/source ratio. No treatment effect was observed in the fruit water content. The Hunter parameter related to red (a*) decreased as a result of high temperature in fruits subjected to the stress from the fully developed green fruit stage (6 DHT). Similarly, in a previous study, the redness of tomato decreased when fruits were ripened off-vine at 32 °C, as a result of the inhibition of lycopene synthesis.8 In our study, the negative effect of high temperature on the red color diminished as the period of exposure to the stress increased. Moreover, in fruits grown 36 and 44 days under high temperature, the value of a* increased above that obtained in control fruits. The analysis of metabolites in control fruits was initially carried out separately in individual trusses (from 3 to 6). However, no differences between trusses were observed in any

a

DHT are mean values for each treatment, with a maximum variability of ±3 days. bDiameter.

replicates per treatment were randomly collected, each one constituted by ten fruits. After the physical parameters had been determined, fruits belonging to the same sample were cut into small pieces (using the whole fruit), powdered with liquid N2, and kept at −80 °C until subsequent analysis. For the extraction of vitamin C, samples were homogenized with EDTA (St. Louis, MO, USA), 0.05% (w/v), and dithiothreitol (SigmaAldrich, Steinheim, Germany). Vitamin C, measured as the sum of ascorbic acid and dehydroascorbic acid, was analyzed using liquid chromatography equipped with a triple quadrupole mass spectrometer detector (Agilent Series 1200, Santa Clara, CA, USA) according to the methodology developed by Fenoll et al.10 For accurate quantification of the samples, the standard addition approach was performed. Ascorbic acid standard was purchased from Sigma-Aldrich (SigmaAldrich, Steinheim, Germany) (purity >99%). Carotenoids were extracted according to the method of Böhm11 with methanol/tetrahydrofuran (1/1, v/v) containing 0.1% BHT (Sigma-Aldrich, St. Louis, MO, USA) and using β-apo-8′-carotenal (Sigma-Aldrich, St. Louis, MO, USA) as internal standard. Carotenoids were determined using a Hewlett-Packard model 1100 HPLC system (Waldbronn, Germany) equipped with a photodiode array UV/vis detector. Separation was achieved in a 250 mm × 4.6 mm i.d., 3 μm Prontosil C30 column (Bischoff, Leonberg, Germany) with methanol (solvent A) and methyl tert-butyl ether (solvent B) as mobile phase. All the solvents (HPLC grade) were supplied by Fisher Chemical (Loughborough, U.K.). The gradient procedure was as follows: (1) initial conditions 15% solvent B and 85% solvent A, (2) a 10 min linear gradient to 15% solvent B, (3) a 20 min linear gradient to 90% solvent B. Elution was performed at a solvent flow rate of 1.3 mL/min with an injection volume of 20 μL and detection at 287 nm for phytoene, 347 nm for phytofluene, and 444 nm for other carotenoids and internal standard. Carotenoids in the samples were identified by comparison of retention times and UV−vis absorptions with those of the corresponding standard or with those reported in the literature. In addition, cis isomers were identified based on their absorption at near 330 or 360 nm and by the Q ratio, defined as the height ratio of the cis peak to the main absorption peak, as previously

Table 2. Mean Weight, Equatorial Diameter, Longitudinal Diameter, Color Hunter Parameters (L*, a*, and b*), Total Soluble Solids, and Water Content (WC) of Tomato Fruits under Different Exposure Periods at 32 °Ca days under high temperature MWb (g) eq diamc (mm) long. diamd (mm) L* a* b* TSSe (°Brix) WCf(%)

0

6

16

22

27

36

44

83.5 cd 60.1 bc 42.0 b 35.5 a 15.1 ab 13.3 a 4.2 ab 94.1

85.7 d 60.7 bc 42.1 b 36.5 a 13.0 a 14.5 ab 4.0 a 94.6

78.1 abcd 57.1 bc 41.7 b 35.3 a 13.6 a 13.5 a 4.1 ab 94.87

67.2 abc 55.4 ab 39.1 ab 36.2 a 15.8 b 14.6 ab 4.0 ab 94.9

60.9 a 50.5 a 37.5 a 36.1 a 16.4 b 14.2 ab 4.2 ab 95.5

63.5 ab 55.5 a 37.7 ab 36.5 a 18.6 c 15.0 b 4.6 bc 93.5

79.5 bcd 60.0 c 43.8 b 38.2 b 26.3 d 17.1 c 4.8 c 94.0

a

Different letters in the same column indicate significant differences between means according to Tukey’s test. Values are means (n = 6). bMean weight. cEquatorial diameter. dLongitudinal diameter. eTotal soluble solids. fWater content. 2379

DOI: 10.1021/jf505507h J. Agric. Food Chem. 2015, 63, 2378−2382

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Journal of Agricultural and Food Chemistry

decreased sink/source ratio due to increased flower abortion. A concentration effect cannot be attributed to the lower fruit water content since no differences in this parameter were observed between treatments. The carotenoids identified and quantified in the tomato samples by HPLC were phytoene, phytofluene, all-translycopene, 13-cis-lycopene, 5-cis-lycopene, lutein, all-trans-γcarotene, all-trans-β carotene, 9-cis-β-carotene, 13-cis-β-carotene, and violaxanthin (Figure 2). The increased temperature,

of the studied metabolites (carotenoids and vitamin C), and so the results of the control treatment are presented as the mean values for the different trusses. The fact that no differences were observed between trusses in control plants can be attributed to (i) fruits from different trusses were collected from different plants, and therefore no modification of the sink/source ratio was influenced by previous harvest before sampling, and (ii) in the growth chamber, where the photoperiod remained unaltered throughout the growing period, differences between trusses are are much less likely to occur than in natural conditions. The effect of high temperature on vitamin C concentration depended on the duration and timing of the stress (Figure 1).

Figure 1. Vitamin C concentration in fruits exposed to temperature stress (32 °C) during increasing time periods. Bars are mean values ± SE (n = 6).

In fruits subjected to 32 °C from the advanced development stages (stage 6 and stage 5, equivalent to 6 and 16 DHT, respectively), vitamin C concentration decreased with regard to control fruits. The negative effect of high temperature on vitamin C decreased as the period of exposure to the stress increased. Thus, fruits grown at a high temperature for 36 days (from stage 4) showed a similar vitamin C content to control fruits. Moreover, increasing the exposure period up to 44 days led to an increase in the vitamin C concentration to above the values obtained in control fruits. The stress caused by high temperatures leads to an alteration of the composition of the fruit through modifications at physiological, biochemical, and molecular levels. At plant level, the increased temperature changes the distribution of photoassimilates among plant organs, increasing biomass translocation to fruits at the expense of vegetative growth.12 On the other hand, temperatures above the optimum values can directly alter metabolite synthesis/degradation processes. In particular, ascorbate accumulation is limited by high temperatures, which reduce ascorbate synthesis and/or favor ascorbate degradation through oxidation due to intensified ascorbate peroxidase and ascorbate oxidase activities and a depression of the enzyme dehydroascorbate reductase.14 The increase of vitamin C concentration observed after longer periods at high temperature suggests an adaptation of the plant metabolism to high temperature and/or a restoration of the ascorbate synthesis processes during the time intervals in which the temperature decreases along the photoperiod (night). Finally, the vitamin C content was higher in fruit exposed to a high temperature from flowering than in control fruits, probably due to a concentration effect as a result of a

Figure 2. HPLC-DAD chromatogram of carotenoids in cv. Velasco recorded at 444, 287, and 347 nm. Peak identification: (1) violaxanthin, (2) lutein, (3) internal standard, (4) 13-cis-β-carotene, (5) all-trans-β-carotene, (6) 9-cis-β-carotene, (7) all-trans-γ-carotene, (8) 13-cis-lycopene, (9) all-trans-lycopene, (10) 5-cis-lycopene, (11) phytoene, and (12) phytofluene.

when imposed in the fully developed green fruit stage (stage 5), lowered the concentration of total lycopene (calculated as the sum of all-trans, 13-cis, and 5-cis lycopene isomers) in the mature fruit (Figure 3A). This decrease was accompanied by a decrease in the concentration of phytoene and phytofluene (precursors) and an increase in lutein (product) (Table 2 and Figure 4). At earlier stages, the inhibitory effect of temperature on the accumulation of lycopene and its precursors and the stimulatory effect on lutein decreased in proportion to the length of exposure to 32 °C. In the case of fruit subjected to high temperatures since flowering, the phytoene and lycopene concentrations reached higher levels than those observed in the control fruits. Unlike lycopene, the total β-carotene concentration (calculated as the sum of all-trans-, 9-cis-, and 13-cis-βcarotene isomers) was not affected by the temperature increase (Figure 3B). Furthermore, the concentrations of γ-carotene and 2380

DOI: 10.1021/jf505507h J. Agric. Food Chem. 2015, 63, 2378−2382

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Journal of Agricultural and Food Chemistry

product lycopene in fruits subjected to a high temperature for a short period (stage 5). Some authors suggest that the decrease in lycopene as a result of temperature increase may be due to a degradation of this compound toward the formation of βcarotene.8 However, our results also suggest a degradation of lycopene toward the formation of lutein. The feedback control mechanisms and metabolic channeling between each branch of the isoprenoid pathway play a key role in the final concentration of each compound.17 Thus, the fact that the concentration of β-carotene was stable could be linked, on the one hand, to the increased degradation of lycopene and γ-carotene and, on the other, to the decreased catabolism of βcarotene into the formation of violaxanthin, which would also explain the observed decrease in the concentration of the latter compound. An increasing time of exposure to temperature stress reduced the negative effect of temperature on the concentration of phytoene, phytofluene, lycopene, and lutein, suggesting, similarly to that observed in the case of vitamin C, an adaptation of the plant metabolism to high temperature and/or the restoration of carotenoid synthesis processes during the time intervals in which the temperature decreases along the photoperiod. The increase in the total carotenoid content observed in fruits from the stage 1 treatment (Table 3) could also be attributed to a concentration effect resulting from a lower sink/source ratio. In addition to these metabolic changes in the isoprenoid biosynthesis route, temperature stress led to an increase in the concentration of the 13-cis isomer of β-carotene and lycopene. The formation of cis isomers from the all-trans form as a result of increased temperature has previously been described.18 Different lycopene isomers were shown to have different stabilities (5-cis ≥ all-trans ≥ 9-cis ≥ 13-cis > 15-cis > 7-cis > 11cis) due to their molecular energy.19 Although the cis forms are more unstable, cis-lycopene isomers have been shown to be more bioavailable than trans-lycopene probably because of their shorter length and low tendency to form aggregates, which confers greater solubility.20,21 In conclusion, the effect of increased temperature on fruit development and on the concentrations of vitamin C and carotenoids depended closely on the development stage at which the stress was first imposed. In general, increased temperature negatively affected fruit weight and size propor-

Figure 3. Total lycopene (A) and total β-carotene (B) concentrations in fruits exposed to temperature stress (32 °C) during increasing time periods. Bars are mean values ± SE (n = 6).

Figure 4. Summary of carotenoid biosynthesis.

violaxanthin decreased in proportion to the time of exposure to heat stress. According Gautier et al.,8 the enzyme phytoene synthase (PSY), responsible for the formation of phytoene from two molecules of geranylgeranyl diphosphate (GGPP), plays a key role in regulating the biosynthesis of carotenoids. PSY is inhibited by temperature increases, especially at the transcriptional level.15,16 This inhibition could explain the observed decrease in the concentration of phytoene, phytofluene, and its

Table 3. Carotenoid Concentration (μg g−1FW) in Tomato Fruits Exposed to High Temperature (32 °C) during Increasing Time Periodsa days of exposure at high temperature (DHT) compound phytoene phytofluene all-trans-lycopene 13-cis-lycopene 5-cis-lycopene lutein all-trans-γ-carotene all-trans-β-carotene 9-cis-β-carotene 13-cis-β-carotene violaxanthin total carotenoids a

0 16.8 7.8 100.4 4.8 3.3 11.2 3.2 25.7 0.6 0.9 3.1 177.8

6 c bc b a b a c

a d ab

8.5 4.2 78.5 5.2 1.9 12.8 2.8 24.6 0.6 1.0 3.0 143.1

16 a a a ab a ab bc

ab cd a

9.9 5.1 94.9 6.6 1.8 13.8 2.8 25.2 0.7 1.3 2.5 164.6

22 ab ab ab abc a b bc

cd bcd ab

11.4 5.4 99.3 6.4 2.2 13.2 2.3 24.2 0.6 1.2 2.5 168.7

27 ab ab ab abc ab ab ab

ab bc ab

13.5 6.2 111.3 7.1 1.8 13.4 2.1 25.9 0.7 1.4 2.2 185.6

36 bc ab b bc a ab a

cd b b

22.7 6.3 107.2 8.5 2.2 13.7 1.9 24.5 0.7 1.4 1.8 190.9

44 d ab b c ab b a

cd b bc

24.4 6.7 143.6 9.3 1.9 12.2 2.0 21.6 0.5 1.3 1.1 224.6

d c c d ab ab a

d a c

Different letters in the same column indicate significant differences between means. 2381

DOI: 10.1021/jf505507h J. Agric. Food Chem. 2015, 63, 2378−2382

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Journal of Agricultural and Food Chemistry

(7) Bita, C. E.; Zenoni, S.; Vriezen, W. H.; Mariani, C.; Pezzotti, M.; Gerats, T. Temperature stress differentially modulates transcription in meiotic anthers of heat-tolerant and heat-sensitive tomato plants. BMC Genomics 2011, 12, 384. (8) Gautier, H.; Diakou-Verdin, V.; Benard, C.; Reich, M.; Buret, M.; Bourgaud, F.; Poessel, J. L.; Caris-Veyrat, C.; Genard, M. How does tomato quality (sugar, acid, and nutritional quality) vary with ripening stage, temperature, and irradiance? J. Agric. Food Chem. 2008, 56, 1241−1250. (9) Intergovernmental panel on climate change. Third Assessment ReportClimate Change 2001: Synthesis Report. http://www.ipcc. ch. (10) Fenoll, J.; Martinez, A.; Hellin, P.; Flores, P. Simultaneous determination of ascorbic and dehydroascorbic acids in vegetables and fruits by liquid chromatography with tandem-mass spectrometry. Food Chem. 2011, 127, 340−344. (11) Bohm, V. Use of column temperature to optimize carotenoid isomer separation by C-30 high performance liquid chromatography. J. Sep. Sci. 2001, 24, 955−959. (12) de Koning, A. N. M. Quantifying the responses to temperature of different plant processes involved in growth and development of glasshouse tomato. Acta Hortic. 1996, 406, 99−104 http://www. actahort.org/books/406/406_9.htm. (13) Sato, S.; Peet, M. M.; Thomas, J. F. Determining critical preand post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. J. Exp. Bot. 2002, 53, 1187−1195. (14) Rosales, M. A.; Ruiz, J. M.; Hernandez, J.; Soriano, T.; Castilla, N.; Romero, L. Antioxidant content and ascorbate metabolism in cherry tomato exocarp in relation to temperature and solar radiation. J. Sci. Food Agric. 2006, 86, 1545−1551. (15) Bramley, P. M. Regulation of carotenoid formation during tomato fruit ripening and development. J. Exp. Bot. 2002, 53, 2107− 2113. (16) Fraser, P. D.; Bramley, P. M. The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res. 2004, 43, 228−265. (17) Poiroux-Gonord, F.; Bidel, L. P. R.; Fanciullino, A.-L.; Gautier, H.; Lauri-Lopez, F.; Urban, L. Health benefits of vitamins and secondary metabolites of fruits and vegetables and prospects to increase their concentrations by agronomic approaches. J. Agric. Food Chem. 2010, 58, 12065−12082. (18) Takehara, M.; Nishimura, M.; Kuwa, T.; Inoue, Y.; Kitamura, C.; Kumagai, T.; Honda, M. Characterization and thermal isomerization of (all-E)-lycopene. J. Agric. Food Chem. 2014, 62, 264−269. (19) Chasse, G. A.; Mak, M. L.; Deretey, E.; Farkas, I.; Torday, L. L.; Papp, J. G.; Sarma, D. S. R.; Agarwal, A.; Chakravarthi, S.; Agarwal, S.; Rao, A. V. An ab initio computational study on selected lycopene isomers. J. Mol. Struct.: THEOCHEM 2001, 571, 27−37. (20) Melendez-Martinez, A. J.; Paulino, M.; Stinco, C. M.; MapelliBrahm, P.; Wang, X. D. Study of the time-course of cis/trans (Z/E) isomerization of lycopene, phytoene, and phytofluene from tomato. J. Agric. Food Chem. 2014, 62, 12399−12406. (21) Boileau, A. C.; Merchen, N. R.; Wasson, K.; Atkinson, C. A.; Erdman, J. W. Cis-lycopene is more bioavailable than trans-lycopene in vitro and in vivo in lymph-cannulated ferrets. J. Nutr. 1999, 129, 1176−1181.

tionally to the length of exposure. However, tomatoes subjected to the stress from the flowering stage showed similar weights and sizes to control fruits, due to a higher incidence of flower abortion and the subsequent weight increase in the remaining fruits. As regards nutritional quality, exposure to the increased temperature of 32 °C over a short period of time (beginning when fruit were in the last developing stages) caused a decrease of the concentration of vitamin C and lycopene but did not affect the β-carotene concentration. Changes in the concentrations of other carotenoids can be explained by possible metabolic channeling between the different isoprenoid biosynthetic pathway branches. The negative effect of high temperature on vitamin C and lycopene diminished as the period of exposure to the stress increased, reaching values similar to those obtained in control fruits, or even higher if fruits were under temperature stress since flowering. These results show the ability of the tomato plants to adapt to temperature stress, being able to restore the concentrations of these metabolites after longer periods at high temperature. These results contribute to a better understanding of the effect of increased air temperature, as may be expected as a result of global warming, on the functional quality of tomato, allowing a more precise evaluation of temperature stress on the vitamin C and carotenoid concentrations of the fruit.

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AUTHOR INFORMATION

Corresponding Author

*Instituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA), c/ Mayor s/n, La Alberca, 3150 Murcia, Spain. E-mail: mpilar.fl[email protected]. Phone: +34 968 366804. Fax: +34 968 366792. Funding

This research has been supported by INIA (Project RTA201000119-00-00 and a predoctoral fellowship). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors are grateful to Inmaculada Garrido González, Juana Cava Artero, and Marı ́a V. Molina Menor for technical assistance.

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REFERENCES

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DOI: 10.1021/jf505507h J. Agric. Food Chem. 2015, 63, 2378−2382