Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics

Scientia Horticulturae 165 (2014) 106–110

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Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics B. Pezzarossa a,∗ , I. Rosellini a , E. Borghesi b , P. Tonutti c , F. Malorgio b a b c

Institute of Ecosystem Study, CNR, Pisa, Italy Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy Institute of Life Science, Scuola Superiore Sant’Anna, Pisa, Italy

a r t i c l e

i n f o

Article history: Received 14 May 2013 Received in revised form 4 October 2013 Accepted 22 October 2013 Keywords: Ethylene Fruit ripening Postharvest Quality Selenium Shelf-life

a b s t r a c t Selenium appears to be effective in promoting plant development and delaying the onset of senescence. Besides the effects on the metabolism and physiology of different crops, controlled increases in Se concentrations enhance the health-related properties of the produce. To study the effects of selenium on fruit composition and ripening physiology, an experiment was carried out on tomato (Solanum lycopersicum) plants grown in hydroponics. Sodium selenate was added to the nutrient solution at a rate of 0 (control) and 1 mg Se L−1 . The selenium added to the nutrient solution was absorbed by the roots, and the Se concentration was higher in leaves than in fruits. The addition of Se did not significantly influence the cumulative yield of tomato plants, but a delay in the onset of fruit ripening was detected, and the harvesting of control plants began earlier than in Se-treated plants. The addition of Se did not significantly affect the qualitative parameters with the exception of ␤-carotene content, which was lower in red ripe fruit treated with selenium. Since ␤-carotene accumulation is a ripening-related event in tomato, the lower amount of this compound may be associated with a general delay of ripening. This is confirmed by the reduced biosynthetic rate of ethylene, observed in Se-treated tomatoes, which also showed a reduced rate in colour change. This thus confirmed that ripening-related processes, such as the degradation of chlorophyll and the synthesis of carotenoids, are affected by selenium - with potential benefits in terms of storage and shelf-life. Our results showed that 100 g of tomato hydroponically grown with a nutrient solution supplemented with Se provided a total of 58 ␮g Se. Thus, the daily consumption of 100 g of enriched tomato does not lead to Se toxicity, but can even provide a rational Se supplementation. This suggests that the addition of Se in a nutrient solution is useful for producing tomatoes with greater beneficial properties for human health. © 2013 Elsevier B.V. All rights reserved.

1. Introduction The quality of fruit and vegetables at harvest and during storage is greatly affected by agronomic factors such as fertilisation, water management, and hormone treatments (Lin and Jolliffe, 1996; Gelly et al., 2003). Considering plant nutrition, both essential and nonessential macro and microelements exert marked effects on fruit growth, development, composition, and quality traits, as well as the incidence of diseases and physiological disorders both on- and off-plant (Kirkby and Römheld, 2004; Fageria, 2009; Savvas et al., 2008; Gong et al., 2011). Several papers report the effects of essential micronutrients (Fageria et al., 2002; Li and Wu, 2009, Esringüa et al., 2011). However there are few works on non-essential elements, including selenium (Alcaraz-Lopez et al., 2003; Hu et al., 2003; Rios et al., 2010), even though there is no general agreement

∗ Corresponding author. Tel.: +39 50 6212488; fax: +39 50 6212473. E-mail address: [email protected] (B. Pezzarossa). 0304-4238/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scienta.2013.10.029

regarding the classification of Se as non essential in plants. Its beneficial role has been considered in species capable of accumulating high amounts of Se and that need Se for their normal growth, and in some crops to counteract oxidative stress (Terry et al., 2000; Djanaguiraman et al., 2005). Due to its antioxidant properties, Se increased stress tolerance in lettuce and ryegrass (Hartikanen et al., 2000; Xue et al., 2001) and had positive effects on photooxidative stress resistance in potato (Seppanen et al., 2003), suggesting that Se activates protective mechanisms that can alleviate oxidative stress in the chloroplasts. Through mechanisms that have not yet been fully understood, Se appears to be effective in delaying plant senescence, thus decreasing postharvest loss due to enhanced antioxidation associated with an increase in glutathione peroxidase activity (Hartikainen et al., 2000; Xue et al., 2001). In lettuce and chicory, Se added to the nutrient solution decreased the production of ethylene and PAL activity, consequently improving the quality of leafy vegetables and the shelf life in both species (Malorgio et al., 2009). The addition of selenate to the soil induced a reduced growth, a delay in the onset of senescence, and a

B. Pezzarossa et al. / Scientia Horticulturae 165 (2014) 106–110

prolonged vegetative period in tomato plants (Pezzarossa et al., 1999a). In crops such as peach and pear, the enhanced selenium concentration, obtained through spraying the canopy, slowed down the rate of fruit softening, thus increasing the shelf-life (Pezzarossa et al., 2012a). Besides the effects on metabolism and physiology of the different crops, increases in Se concentrations enhance the healthrelated properties of the produce. In fact Se, as a component of the amino acid selenocysteine, which is present in several enzymes such as glutathione peroxidase, tetraiodothyronine 5’ deiodinase and in selenoprotein P, has been considered to be an essential trace element, a natural antioxidant, and an effective anticarcinogenic agent both in humans and animals (Rotruck et al., 1973; Pallaud et al., 1997; Ramauge et al., 1996). There is increasing evidence that improving Se status without exceeding the toxic threshold may benefit long-term health, especially by lowering the risk of cancer (Finley, 2007). The consumption of Se-enriched plants is a good way to supplement selenium, because of the higher bioavailability of the organic forms. Effective ways to increase Se levels in edible crops include spraying the plant with selenium solution (Hu et al., 2003; Kopsell et al., 2009; Pezzarossa et al., 2012a), adding selenite or selenate to soil (Bisberg and Gissel-Nielsen, 1969; Gissel-Nielsen and Bisberg, 1970; Pezzarossa et al., 1999a; Hu et al., 2003; Carvalho et al., 2003; Lee et al., 2007; Rios et al., 2008), and growing hydroponic cultivation in a nutrient solution containing Se (Tsuneyoshi et al., 2006; Malorgio et al., 2009; Ferrarese et al., 2012). Hydroponics, managed as a closed system, enables Se to be well controlled, which is necessary in order to avoid hyperaccumulation and the consequent toxic effects. It can also be used for improving the quality and the shelf-life of fruit with adequate Se concentrations for the human diet. Here we report the results of trials on tomato plants using a hydroponic solution supplemented with Se. The focus was on the effects of the treatment on fruit composition at harvest and ripening physiology.

2. Materials and methods The experiment was conducted in a temperature-controlled greenhouse located in Pisa, Italy (lat. 43◦ 40 N). The plants (Solanum lycopersicum cv. Red Bunch) were hydroponically grown during the spring-summer season, May 5 - July 26. The minimum temperature and ventilation air temperature inside the glasshouse were 13 ◦ C and 27 ◦ C, respectively; the maximum temperature was 30–32 ◦ C. The maximum photosynthetic photon flux density (PPFD) ranged from 600 to 800 ␮mol m−2 s−1 ; the mean value of daily global radiation (R) was 8.4 MJ m−2 . Seedlings were transplanted 50 days after sowing (May 5) into rock wool slabs (100 cm long × 15 cm wide × 7.5 cm tall) placed on two benches. The plants were grown vertically with a single stem at a density of three plants m−2 , and pollination was favoured by mechanical vibration of the flower clusters. Thirty plants were placed on each bench, but only four plants for each treatment were selected for the analyses, based on their similar behaviour and appearance. Sodium selenate was added to the nutrient solution at a rate of 0 (control) and 1 mg Se L−1 two weeks after transplanting (May 21), in two different benches. Drip irrigation was carried out using a nutrient solution with electrical conductivity (EC) 3.5 dS m−1 and pH 6.5. The exhaust nutrient solution was discharged after three weeks or whenever the EC was higher than 6 dS m−1 . The composition of the nutrient solution was as follows: 14 N–NO3 , 1.25 P, 10.7 K, 5 Ca, 1.6 Mg, 9.5 Na, 8.0 Cl, 2.7 S, 0.04 Fe (concentrations are expressed in

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Table 1 Total Se content, expressed as ␮g Se per g of dry weight, in the leaves and in the red fruit from all trusses, and from lower and higher trusses of tomato plants (cv. Red Bunch) treated at 0 and 1 mg Se L−1 . Values with the same letter in the same column are not statistically different for p ≤ 0.05%. Se added (mg Se L−1 )

0 1

Se content (␮g Se g−1 ) DW Leaf

Red fruit all trusses

Red fruit lower trusses

Red fruit higher trusses

0.1 a 29.8 b

0.1 a 10.33 b

0.02 a 10.28 b

0.1 a 11.46 b

mmol L−1 ). Micronutrients were added at Hoagland’s concentration (in ␮mol L−1 : 40 B, 40 Fe, 1 Cu, 5 Zn, 10 Mn). The tomato fruits on each truss were harvested when 50% of the fruits of the truss were at the red ripe stage, corresponding to an average soluble solid content (SSC) of 4.6◦ Brix and titratable acidity of 0.65%. Harvests were performed on July 5, 9, 11, 15, 20 and 26. Lateral shoots and the leaves below the bottommost truss with ripening fruits were regularly removed. Fresh and dry matter weights of leaves and fruits were recorded. The harvest index (HI) was obtained by dividing the dry matter weight of tomato fruits by the plant’s total dry matter weight. Soluble solid content (SSC) was directly determined in the fruit juice using a digital refractometer (model 53011, Turoni, Italy). Titratable acidity was determined using NaOH 0.1N to the endpoint of pH 8.2 and expressed as citric acidity percentage. In addition, the taste index and maturity were calculated using the equation proposed by Navez et al. (1999) starting from the Brix and the titratable acidity values as indicated in Herdandez Suarez et al. (2008): maturity = ◦ Brix/acidity taste index = (◦ Brix/20 × acidity) + acidity Ethylene production was measured in the controls and treated fruits at harvest (performed on July 12) and throughout the nineday postharvest period at 22 ◦ C. Five fruits were placed in 100 ml glass tubes (Pyrex, France) closed with holed plastic screw caps, and supplied with caoutchouc rubber septa. The analisys were performed as described in Malorgio et al., 2009. Carotenoid (lutein, lycopene, ␤-carotene) was extracted following Giuntini et al. (2005), partially modified. The measurements were carried out by HPLC (Jasco, Tokyo, Japan) consisting of a low pressure gradient pump with a four-solvent model PU-2089 UV–Vis detector and a multichannel UV–2077. A Nucleodur C18 100 (5 ␮m, 250 × 4.6 mm) column was used, with an injection volume of 20 ␮L (Borghesi et al., 2011). For the analyses of Se, content leaf and fruit samples were ovendried at 50 ◦ C for 1 week and then ground in a mortar. Total selenium content was determined after digestion with nitric and perchloric acids and reduction by hydrochloric acid, following Zasoski and Burau (1977). The digests were analyzed by hydride generation atomic absorption spectrophotometry (Varian VGA 77). The Se reference standards, rice flour SRM 1567 (Se content 1.23 ± 0.09 mg kg−1 with a recovery of 92%) and San Joaquin soil SRM 2709 (Se content 1.57 ± 0.08 mg kg−1 with a recovery of 91%), were obtained from the U.S. National Institute of Standards and Technology. Glass tubes containing only the chemical reagents were used as blanks for analytical quality controls in order to constantly monitor for Se contamination in the chemical hood. 3. Results and discussion The selenium added to the nutrient solution was absorbed by the roots and accumulated both in the leaves and fruits (Table 1). As already observed in previous experiments (Pezzarossa et al., 1999a, 1999b) selenium concentration, expressed on a dry weight

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2500

Control

a

1 mg Se L-1

Con trol

1000

1 mg Se Laa 1

a 800

a yield (g plant-1)

yield (g plant -1)

2000

1500

a

a

a

1000

a a a

500

b

0 0

5

b

a

600

a

a a

b 10

15

20

25

0

July

5

b b 10

15

20

25

30

July

Fig. 1. Cumulative yield (weight of total detached fruit, g plant−1 ) detected at different harvest time (i.e. July 5, 9, 11, 15, 20 and 26). Harvest was performed when about 50% of the fruits of the truss were at the red ripe stage. Data are the means of 4 replicates ± SE. Values with the same letter are not statistically different for p ≤ 0.05%.

basis, was higher in the leaves than in the fruits. Fruits from the lower trusses accumulated the same amount of Se as fruits from the higher trusses. The addition of Se did not significantly influence the cumulative yield of tomato plants (Fig. 1). However, harvesting of control plants began earlier than Se-treated plants. The delay in the onset of fruit ripening was evident considering that the first harvest (about 150 g) in the Se-treated plants was performed on July 12, when a cumulative yield of almost 1 Kg had already been achieved with the control plants and two detachments had already been performed on July 5 and 9. There was a significant difference in fruit yield between the controls and treated plants on July 15, whereas similar values of cumulative yield were detected on July 20 and 26 (Fig. 1). Total and commercial yield, average fruit weight and number of fruits per plant did not differ between the controls and treated plants (Table 2). The addition of Se did not even affect the qualitative parameters, i.e. dry matter content, soluble solid content, titratable acidity, and the taste index measured in the fruits at the red-ripe stage of the second truss in both controls and treated plants. The taste index, calculated starting from the ◦ Brix and acidity values, was unaffected by the selenium treatment and was higher than 0.7 in both treatments (Table 2), indicating that the tomato analyzed was of good quality. In fact, Navez et al. (1999) consider tomato as having little taste when this index is lower than 0.7. Lycopene and lutein content were unaffected by the selenate treatment, which resulted in a lower ␤-carotene content in fruit at the red stage (Table 2). In tomatoes, the content of ␤-carotene Table 2 Production results and qualitative characteristics of fruit in tomato plants (cv. Red Bunch). Data are the means of 4 replicates. Values with the same letter in the same row are not statistically different for p ≤ 0.05%. Se added (mg Se L−1 )

Parameters

Total yield Fruit weight Fruit per plant Commercial yield Solid content Soluble solid content (SSC) Titratable acidity Taste index Maturity index Lycopene Lutein ␤-carotene Harvest Index (HI)

b

0

30

a

a

200

b

a

400

−1

g plant G Number g plant−1 % ◦ Brix meq citric acid

␮g g−1 DW ␮g g−1 DW ␮g g−1 DW

0

1

2167 a 17.8 a 102 a 1830 a 6.2 a 5.5 a 0,53 a 1.04 a 10.4 a 15.7 a 1.34 a 4.1 a 0.83 a

2084 a 17.3 a 109 a 1880 a 6.3 a 5.9 a 0,51 a 1.10 a 11.7 a 24.1 a 0.7 a 1.96 b 0.77 a

Fig. 2. Cumulative yield (g plant−1 ) of detached red fruit detected at different harvest time (i.e. July 5, 9, 11, 15, 20 and 26). Harvest was performed when about 50% of the fruits of the truss were at the red ripe stage. Data are the means of 4 replicates ± SE. Values with the same letter are not statistically different for p ≤ 0.05%.

has been shown to increase from the green to the fully ripe stage (Fraser et al., 1994). Sams et al. (2011) reported that, in Arabidopsis, treatment with Se down-regulates the expression of phytoene synthase, a key step at the beginning of the carotenoid biosynthesis. In tomato fruit, other carotenoid genes and/or enzymes may be affected, directly or indirectly, by Se. This could be the case for example of lycopene cyclases, which is responsible for the formation of carotenes and lutein from lycopene. Since ␤-carotene accumulation is a ripening-related event in tomato (Giovannoni, 2001) and its formation from lycopene appears to be principally under transcription regulation (Fraser et al., 2007; Lee et al., 2012), the lower amount of this compound detected in Se-enriched red ripe fruit may be associated with a general delay in ripening and with some of the associated transcriptional events. This is reinforced by the observation that in cv Ailsa Craig ripening tomatoes, ␤-carotene reaches its maximum earlier than phytoene and lycopene (Alba et al., 2005) and by our data concerning the harvest time of red fruit. A shift of about 10 days in the onset/evolution of ripening was observed, as demonstrated by the lower number of red fruits harvested at the four initial sampling dates (Fig. 2). An effect of Se on ripening physiology is also possible considering the evolution of ethylene biosynthesis in fruit harvested at the red-ripe stage and kept at 22 ◦ C for 9 days. Compared to the controls, which showed a decreasing trend throughout the experimental period, Se-enriched red fruit detached on July 12 produced much lower amounts of the hormone at harvest and during the postharvest phase (Fig. 3). In ripening tomato, the ethylene climacteric rise takes place at the MG-breaker transition, reaching the highest biosynthetic values at the pink-red stage when a decreasing trend is then observed (Van de Poel et al., 2012). In our experiment, ethylene evolution was only analysed in red fruit (when harvested and throughout the postharvest phase), however, compared to control, a reduced biosynthetic rate was observed in tomatoes supplied by the Se-enriched nutrient solution. This is in agreement with our previously published data (Pezzarossa et al., 1999a) which reported a decrease in ethylene production in Se treated tomatoes cv UC82B grown in pots containing loam soil. Growing the model species Arabidopsis on growth plates with a 3.2 ppm selenate concentration negatively affected plant development, moreover in roots and shoots it led to the up-regulation of various genes regulating the synthesis (e.g. ACC synthase) and signaling of ethylene (Van Hoewyka et al., 2008). It is likely that high levels of Se, which negatively affect plant

B. Pezzarossa et al. / Scientia Horticulturae 165 (2014) 106–110

8

Con trol

a

1 mg Se L-1

Ethylene (nl/g/h)

7

a

6

a

5

a

4 3 2

b

b

1

b

a

b

b

0 12

10

14

16 July

18

20

22

Fig. 3. Ethylene evolution in fruits from lower (1 and 2) trusses detached at red stage on July 12 and kept at 22 ◦ C for 9 days. Data are the means of 4 replicates ± SE. Values with the same letter are not statistically different at p ≤ 0.05%.

growth, induce stress responses where ethylene (and other hormones or signaling molecules) is involved, and act as a prooxidant (Hasanuzzaman et al., 2010). At lower concentrations, such as those used in our trials, Se may have exerted anti-oxidant and antisenescence effects, as demonstrated in lettuce (Xue et al., 2001) and soybean (Djanaguiraman et al., 2005), by also interfering directly or indirectly with the biosynthesis of ethylene. The latter is commonly considered an ‘aging’ hormone, as it accelerates and is sometimes required for ripening, senescence, and abscission (Schaller, 2012). The ripening delay and anti-senescence effects of Se are evident when evaluating the evolution of fruit pigmentation after detachment over a 30-day storage period at 22 ◦ C (Fig. 4). In fact, Seenriched fruit showed a reduced rate in colour change, confirming that ripening-related processes, such as the degradation of chlorophyll and the synthesis of carotenoids, are affected by this element, with potential benefits in terms of storage and shelf-life. A final consideration concerns the nutritional and health-related issues of Se-enriched tomatoes. The German and Austrian Nutrition Society along with the Swiss Nutrition Association recommended an adequate daily intake for selenium ranging from 30 to 70 ␮g d−1 for adult men and women. The tolerable dose for adults was set at 400 ␮g d−1 . Considering that the average total selenium content in the treated tomato fruits was 10.33 ␮g Se g−1 dry weight and the dry matter content was 5.65%, our results showed that 100 g of tomatoes hydroponically grown with nutrient solutions containing 1 mg Se L−1 provided a total of 58 ␮g Se. Thus, the daily Control

1 mg Se L-1

120

a

100

a

% red fruit

80 60

b

b

b

b

a

a

b a a

40

a

a

a

a

a 20

a

0 0

2

a 5

a 7

a 12

14

16

19

21

26

30

days from harvest (0=July 9) Fig. 4. Evolution of ripening in tomato fruit of plants treated at 0 and 1 mg Se L−1 . Ripening is expressed as a percentage of red fruits present on the trusses. The colorimetric evaluation was performed for 30 days after harvest on fruits stored at 22 ◦ C. Bars indicate ± SE.

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consumption of 100 g of enriched tomato would not lead to Se toxicity, but could even provide Se supplementation. This suggests that the addition of Se in a nutrient solution is a useful system for producing Se-enriched tomatoes. However, the Se levels are also dependent on the intake of this nutrient from other food sources, thus a consumption higher than 100 g of fresh tomatoes supplemented with 1 mg Se L−1 would not be wise. Our previous experiments have shown that the addition of 0.5 mg Se L−1 in tomato plants grown in hydroponics induced a lower accumulation of selenium in fruits, i.e. 8 g Se/100 g fresh weight (Pezzarossa et al., 2012b). In this case the consumption of tomatoes could be higher without a toxicity risk. However, improving human health by increasing the consumption of Se-enriched food requires a thorough understanding and integration of the agricultural and nutritional chemistry of Se. In conclusion, we believe that our results further support the hypothesis that selenium (at the tested concentration) may modulate fruit development, in particular the ripening process, possibly through its anti-oxidant and anti-senescence properties with beneficial effects in terms of post-harvest commercial life. Fully understanding how the molecular and biochemical mechanisms are directly or indirectly affected by selenium in fruit tissues at ripening and during the postharvest phase should help considerably in optimizing the treatment procedures and protocols. References Alba, R., Payton, P., Fei, Z., McQuinn, R., Debbie, P., Martin, G.B., Tanksley, S.D., Giovannoni, J.J., 2005. Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17 (11), 2954–2965. Alcaraz-Lopez, C., Botia, M., Alcaraz, C.F., Riquelme, F., 2003. Effects of foliar sprays containing calcium, magnesium and titanium on plum (Prunus domestica L.) fruit quality. J. Plant. Physiol. 160, 1441–1446. Bisberg, B., Gissel-Nielsen, G., 1969. The uptake of applied selenium by agricultural plants. I. The influence of soil type and plant species. Plant Soil 31, 287–298. Borghesi, E., Gonzales-Miret, M.L., Escudero-Gilete, M.L., Malorgio, F., Heredia, F.J., Melendez-Martinez, A.J., 2011. Effects of salinity stress on the carotenoid, anthocynins, and color of diverse tomato genotypes. J Agric. Food Chem. 59, 11676–11682. Carvalho, K.M., Gallardo-Williams, M.T., Benson, R.F., Martin, D.F., 2003. Effects of selenium supplementation on four agricultural crops. J Agric. Food Chem. 51, 704–709. Djanaguiraman, M., Devi, D.D., Shanker, A.K., Sheeba, J.A., Bangarusamy, U., 2005. Selenium—an antioxidative protectant in soybean during senescence. Plant Soil 272 (1/2), 77–86. Esringüa, A., Turana, M., Gunesa, A., Es¸itkenb, A., Sambo, P., 2011. Boron application improves on yield and chemical composition of strawberry. Acta Agric. Scand. 61 (3), 245–252. Fageria, N.K., Baligar, C., Clark, R.B., 2002. Micronutrients in crop production. Adv. Agron. 77, 185–268. Fageria, N.K., 2009. The Use of Nutrients In Crop Plants. CRC Press, Francis & Taylor Group, Boca Raton, FL. Ferrarese, M., Mahmoodi Sourestani, M., Quattrini, E., Schiavi, M., Ferrante, A., 2012. Biofortification of spinach plants applying selenium in the nutrient solution of floating system. Veg. Crops Res. Bull. 76, 127–136. Finley, J.W., 2007. Increased intakes of selenium-enriched foods may benefit human health. J. Sci. Food. Agric. 87, 1620–1629. Fraser, P.D., Truesdale, M.R., Bird, C.R., Schuch, W., Bramley, P.M., 1994. Carotenoid biosynthesis during tomato fruit development. Plant Physiol. 105, 405–413. Fraser, P.D., Enfissi, E.M., Halket, J.M., Truesdale, M.R., Yu, D., Gerrish, C., Bramley, P.M., 2007. Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19, 3194–3211. Gelly, M., Recasens, I., Girona, J., Mata, M., Arbones, A., Rufat, J., Marsal, J., 2003. Effects of stage II and postharvest deficit irrigation on peach quality during maturation and after cold storage. J. Sci. Food Agric. 84, 563–570. Giovannoni, J.J., 2001. Molecular regulation of fruit ripening. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 725–749. Gissel-Nielsen, G., Bisberg, B., 1970. The uptake of applied selenium by agricultural plants. 2. The utilization of various selenium compounds. Plant Soil 32, 382–396. Giuntini, D., Graziani, G., Lercari, B., Fogliano, V., Soldatini, G.F., 2005. Changes in carotenoid and ascorbic acid contents in fruit of different tomato genotypes related to the depletion of UV–B radiation. J. Agric. Food Chem. 53, 3174–3181. Gong, X., Qu, C., Liu, C., Hong, M., Wang, L., Hong, F., 2011. Effects of manganese deficiency and added cerium on nitrogen metabolism of maize. Biol. Trace Elem. Res. 144 (1-3), 1240–1250. Hartikainen, H., Xue, T., Pironen, V., 2000. Selenium as an antioxidant and prooxidant in ryegrass. Plant Soil 225, 193–200.

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