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      Editorial: Bioactive Compounds Biosynthesis and Metabolism in Fruit and Vegetables

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          Abstract

          Bioactive Compounds Biosynthesis and Metabolism in Fruit and Vegetables Fruit and vegetables are considered to be among the most important sources of bioactive compounds with proven beneficial effect on human diet. Tomato has been evolved as a model crop to study both fruit ripening pattern as well as for understanding how different environmental and agricultural factors can enhance the accumulation of bioactive compounds. The concentration of bioactive compounds is highly dependent on the crop species, cultivar/genotype, agronomic management, preharvest environmental conditions, and postharvest management practices (Toscano et al.). Bioactive compounds in fruit and vegetables are of consumer interest for their potential benefit to the health, especially in counteracting several diseases related to aging and stress. However, the bioactive molecules also have preservation properties that extend the shelf life of the produce. Postharvest technologies and storage conditions can reduce the degradation of bioactive compounds and some industrial operation can even promote their accumulation. The systematic screening of key bioactive compounds with high content in a wide range of germplasm and the restoration of key genes and gene clusters from wild species and/or landraces both are important for reducing the loss of agro-biodiversity and the creation of a “gene pool” that can be exploited in future breeding programs toward the release of new cultivars with added nutraceutical value (Manganaris et al., 2018). Furthermore, the understanding how the accumulation of bioactive compounds can be enhanced or preserved is crucial for improvement of crop and product quality (Toscano et al.). The availability of advanced molecular tools allows fast and accurate transcriptome profiling that can help in the identification of the main gene clusters that are activated or repressed under different conditions. Such information coupled with the big data from metabolomics studies will be useful both for preharvest and postharvest management of produce with high nutritional value. Impact of Genotype and Significance of ‘Old-Fashioned’ Cultivars on Bioactive Content Bioactive compounds show wide variations among different species. Several studies have reported that ancient or old varieties accumulate higher concentration of bioactive compounds that have been linked to their adaptation to different environmental conditions (García-Mier et al., 2013; Manganaris et al., 2018). The accumulation of bioactive compounds can serve as defenses against biotic and abiotic stresses. Local varieties of tomato (Solanum lycopersicum L.) grown in Tuscany showed higher polyphenols, flavonoids, and carotenoids compared with commercial ones (Berni et al.). Similar results have been reported in onion (Allium cepa L.) and sweet cherry [Prunus avium L., (Berni et al.)]. In the meantime, breeding projects are targeting toward the release of new cultivars with enhanced bioactive content, as this is the case for tomatoes (Lenucci et al., 2006). Recently, interest for the black tomatoes has been attributed to the high carotenoid and anthocyanin contents. The ‘Sun Black’ tomato, a result of a 20-years breeding activity, derived from wild tomato species, such as Solanum chilense, Solanum cheesmaniae, Solanum lycopersicoides, and Solanum habrochaites, through introgression with cultivated genotypes (Mazzucato et al., 2013). A comparative study showed that the anthocyanins-enriched ‘Sun Black’ tomato had an almost double concentration of phenolics and carotenoids at the ripe stage compared to the wild type. Color is often an indicator of the composition and concentration of the bioactive compounds. In tomatoes and watermelon, the red color is due to the accumulation of lycopene while the yellow color due to β-carotene. The concentration of these two carotenoids can induce different flesh and skin colors (Ilahy et al.). These compounds are also substrates for volatile biosynthesis, contributing to fruit aroma with direct effect on produce quality (Ilahy et al.). Environmental Conditions Affect the Accumulation of Bioactive Compounds Environmental conditions can positively or negatively affect the concentration of bioactive molecules in different horticultural produce. Tomato fruits obtained from plants exposed to high salinity conditions (60 or 120 mM NaCl) showed a reduction of antioxidant capacity and several secondary metabolites such as lycopene and phenols (Moles et al.). Environmental conditions including altitude, temperature, and light can influence bioactive compound accumulation. A study carried out on blueberry (Vaccinium corymbosum L.) grown in different altitudes, was shown that lower altitudes induced an early ripening and a higher anthocyanin accumulation (Spinardi et al.). Light quality can induce the biosynthesis of different secondary metabolites that can have protective functions against biotic and abiotic stresses. Plants exposed to UV-B treatments have increased phenolic compounds in a dose-response manner. In a study performed in peaches (Prunus persica L.), UV-B treatments applied for 1 or 3 h enhanced several phenolic compounds. The employment of UV-B was also studied as priming for preventing the development of Monilinia fructicola fungus (Santin et al.). Treatments applied for different durations indicated that 1 and 3 h of UV-B treatments increased the phenolics in the fruit except near the inoculation point, while around the inoculation point the effect of UV-B treatments were not always consistent depending also on the effects of fungus, the wounding and their interaction (Santin et al.). Hormonal Regulation of Bioactive Compounds There are plant hormones that have bioactive molecules as precursors such as abscisic acid (ABA), auxin, salicylic acid (SA), and melatonin. ABA biosynthesis is derived from the catabolism of carotenoids, while the auxins, SA, and melatonin are synthetized from the chorismite as their precursor. The connecting molecules may explain the cross-talks among them and their roles in the modulation of the growth and the ripening process of both climacteric and non-climacteric fruits (Pérez-Llorca et al.). The protection of plant cells from external environments and biotic or abiotic stresses is partly provided by the cell wall and, in several species, by the cuticular waxes. The major components of cuticular wax are very long chain fatty acids and derived compounds (Trivedi et al.). However, the concentration and composition of these molecules in the cuticular waxes varies among species and within cultivars of the same species. Tomato mutants such as NON-RIPENING (nor) and RIPENING INHIBITOR (rin) have different cuticular waxes (Kosma et al., 2010). These findings suggest that ethylene plays a role in the wax biosynthesis and accumulation. This hypothesis has been confirmed in the apple and orange. At molecular level, it has been shown that many transcription factors are involved in the regulation of wax biosynthesis such as FRUITFULL and TOMATO AGAMOUS-LIKE1 (Trivedi et al.). In particular, the MADS-RIN transcription factor TDR4/FUL1 and its homolog MBP7/FUL2 have high similarity with FRUITFULL of Arabidopsis. This TDR4 transcription factor has been reported to be involved in pigment biosynthesis in tomato fruit. A functional analysis of this gene using virus-induced gene silencing technology (VIGS) demonstrated that the TDR4 gene is effectively involved in the biosynthesis of bioactive molecules. In fact, TDR4-silenced tomatoes showed a strong reduction of amino acids and α-tomatine (Zhao et al.). The collection of articles in this Research Topic demonstrates that the accumulation of bioactive compounds in produce can derive from different environmental, genetic, and agronomic factors. Author Contributions All authors planned the structure of the editorial, contributed in its writing, read and approved the submitted version. Conflict of Interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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          Most cited references5

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          Antioxidant composition in cherry and high-pigment tomato cultivars.

          Fourteen cultivars of cherry tomatoes and four cultivars of high-pigment tomato hybrids were cultivated in southern Italy, and the red-ripe fruits were analyzed for their content in different classes of antioxidants and for their antioxidant activity. Among the different cultivars, significant differences were found between lycopene, beta-carotene, alpha-tocopherol, vitamin C (ascorbic acid and dehydroascorbic acid), and total phenolic and flavonoid contents. LS203 and Corbus appear to be the cultivars with the highest content of lipophilic and hydrophilic antioxidants among cherry tomatoes, respectively. All cultivars of high-pigment tomato hybrids showed an expected exceptionally high lycopene content. Among them, the highest content of lipophilic and hydrophilic antioxidants was found in cv. HLY 13. Hydrophilic and lipophilic antioxidant activities were both significantly influenced by genotype. Such results highlight an existing unexploited variability in tomato germplasm and stress the need to evaluate the biodiversity and to support conventional breeding programs to improve tomato nutritional value.
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            Nutraceutical Characterization of Anthocyanin-Rich Fruits Produced by “Sun Black” Tomato Line

            Tomato (Solanum lycopersicum L.) is one of the most cultivated vegetable in the world and it represents a large source of bioactive compounds, including carotenoids and polyphenols (phenolic acids and flavonoids). However, the concentration of flavonoids in tomato is considered sub-optimal, particularly because anthocyanins are not generally present. Therefore, this crop has been the object of an intense metabolic engineering in order to obtain anthocyanin-enriched tomatoes by using either breeding or transgenic strategies. Some wild tomato species, such as S. chilense and S. cheesmaniae, biosynthesize anthocyanins in the fruit sub-epidermal tissue, and some alleles from those genotypes have been introgressed into a new developed purple tomato line, called “Sun Black” (SB). It is a tomato line with a purple skin color, both in green and in red fruit stages, due to the biosynthesis of anthocyanins in the peel, and a normal red color pulp, with a taste just like a traditional tomato. SB is the result of a breeding programme and it is not a genetically modified (GM) product. We report the chemical characterization and structure elucidation of the attractive anthocyanins found in the peel of SB tomato, as well as other bioactive compounds (carotenoids, polyphenols, vitamin C) of the whole fruit. Using one- and two-dimensional NMR experiments, the two main anthocyanins were identified to be petunidin 3-O-[6″-O-(4‴-O-E-p-coumaroyl-α-rhamnopyranosyl) -β-glucopyranoside]-5-O-β-glucopyranoside (petanin) and malvidin 3-O-[6″-O-(4‴-O-E-p-coumaroyl-α-rhamnopyranosyl)-β-glucopyranoside]-5-O-β-glucopyranoside (negretein). The total anthocyanins in the whole ripe fruit was 1.2 mg/g dry weight (DW); 7.1 mg/100 g fresh weight (FW). Chlorogenic acid (the most abundant phenolic acid) was 0.6 mg/g DW; 3.7 mg/100 g FW. The main flavonol, rutin was 0.8 mg/g DW; 5 mg/100 g FW. The total carotenoid content was 211.3 μg/g DW; 1,268 μg/100 g FW. The total phenolic content was 8.6 mg/g DW; 52.2 mg/100 g FW. The vitamin C content was 37.3 mg/100 g FW. The antioxidant activities as measured by the TEAC and ORAC assays were 31.6 and 140.3 μmol TE/g DW, respectively (193 and 855.8 μmol TE/100 g FW, respectively). The results show the unique features of this new tomato genotype with nutraceutical properties.
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              Novel phenotypes related to the breeding of purple-fruited tomatoes and effect of peel extracts on human cancer cell proliferation.

              The production of anthocyanins in the tomato (Solanum lycopersicum L.) fruit is normally absent or poor, but a number of mutants or introgression lines are known to increase anthocyanin levels in vegetative and reproductive tissues. Through conventional breeding, a genetic combination was obtained with the remarkable phenotype of a deep purple fruit pigmentation, due to an accumulation of anthocyanins on the peel. Such a genotype was named Sun Black (SB) as a consequence of its sensitivity to light induction. When characterized for morpho-agronomic traits, SB plants showed increased fertility. Purple fruits displayed an arrangement of the epicarp cells different from normal tomatoes, a feature that could account for different mechanical properties and shelf-life potential. The SB genotype and, to a lesser extent, its single mutant parents showed the capacity to accumulate anthocyanins in the seedling root when grown under light. This phenotype, which was greatly improved by the addition of sucrose to the germination medium, proved to be useful as selection index and gave new insights for in vitro production of anthocyanin extracts. To assess the nutraceutical potential of purple tomatoes, we tested the activity of SB skin extracts on the proliferation of two human cancer cells lines. Cell proliferation was significantly inhibited by SB extract in a dose-dependent manner. When the bioactivity of SB extracts was compared with that of other anthocyanin-containing fruits or vegetables, a significant "Extract*Line" interaction was evidenced, suggesting a crucial role for the extract composition in terms of anthocyanidins and other eventual cell growth-inhibiting compounds.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                19 February 2020
                2020
                : 11
                : 129
                Affiliations
                [1] 1 Institute of Life Sciences, Scuola Superiore Sant'Anna , Pisa, Italy
                [2] 2 Escola Superior de Biotecnologia, Universidade Católica Portuguesa , Porto, Portugal
                [3] 3 Department of Agricultural Sciences, Biotechnology & Food Science, Cyprus University of Technology , Lemesos, Cyprus
                [4] 4 Department of Agricultural and Environmental Sciences—Production, Landscape, Agroenergy, Università degli Studi di Milano , Milan, Italy
                Author notes

                Edited by: Cai-Zhong Jiang, USDA-ARS, United States

                Reviewed by: David Obenland, San Joaquin Valley Agricultural Sciences Center, United States

                *Correspondence: Antonio Ferrante, antonio.ferrante@ 123456unimi.it

                This article was submitted to Crop and Product Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.00129
                7042200
                eecfa666-1222-4dde-bda6-91f685347877
                Copyright © 2020 Francini, Pintado, Manganaris and Ferrante

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 10 December 2019
                : 28 January 2020
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 6, Pages: 3, Words: 1213
                Categories
                Plant Science
                Editorial

                Plant science & Botany
                carotenoids,phenolics,abiotic stress,vitamin,anthocyanin,breeding,hormonal regulation

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