Next Article in Journal
A Mild and Regioselective Ring-Opening of Aziridines with Acid Anhydride Using TBD or PS-TBD as a Catalyst
Next Article in Special Issue
Antimicrobial Activity of Rhoeo discolor Phenolic Rich Extracts Determined by Flow Cytometry
Previous Article in Journal
Cladribine Analogues via O6-(Benzotriazolyl) Derivatives of Guanine Nucleosides
Previous Article in Special Issue
Antibacterial Activity, Antioxidant Effect and Chemical Composition of Propolis from the Región del Maule, Central Chile
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Molecules
Volume 20
Issue 10
10.3390/molecules201018464
molecules-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Breeding Vegetables with Increased Content in Bioactive Phenolic Acids

by
Prashant Kaushik
1,
Isabel Andújar
1,
Santiago Vilanova
1,
Mariola Plazas
1,
Pietro Gramazio
1,
Francisco Javier Herraiz
1,
Navjot Singh Brar
2 and
Jaime Prohens
1,*
1
Instituto de Conservación y Mejora de la Agrodiversidad Valenciana, Universitat Politècnica de València, Camino de Vera 14, Valencia 46022, Spain
2
Department of Vegetable Science, Chaudhary Charan Singh Haryana Agricultural University, Hisar 125001, India
*
Author to whom correspondence should be addressed.
Molecules 2015, 20(10), 18464-18481; https://doi.org/10.3390/molecules201018464
Submission received: 15 July 2015 / Revised: 30 September 2015 / Accepted: 7 October 2015 / Published: 9 October 2015
(This article belongs to the Special Issue Recent Advances in Plant Phenolics)
Browse Figures
Versions Notes

Abstract

:
Vegetables represent a major source of phenolic acids, powerful antioxidants characterized by an organic carboxylic acid function and which present multiple properties beneficial for human health. In consequence, developing new varieties with enhanced content in phenolic acids is an increasingly important breeding objective. Major phenolic acids present in vegetables are derivatives of cinnamic acid and to a lesser extent of benzoic acid. A large diversity in phenolic acids content has been found among cultivars and wild relatives of many vegetable crops. Identification of sources of variation for phenolic acids content can be accomplished by screening germplasm collections, but also through morphological characteristics and origin, as well as by evaluating mutations in key genes. Gene action estimates together with relatively high values for heritability indicate that selection for enhanced phenolic acids content will be efficient. Modern genomics and biotechnological strategies, such as QTL detection, candidate genes approaches and genetic transformation, are powerful tools for identification of genomic regions and genes with a key role in accumulation of phenolic acids in vegetables. However, genetically increasing the content in phenolic acids may also affect other traits important for the success of a variety. We anticipate that the combination of conventional and modern strategies will facilitate the development of a new generation of vegetable varieties with enhanced content in phenolic acids.

1. Introduction

Plant breeding programs have mostly concentrated on yield improvement, resistance to diseases, tolerance to abiotic stresses, longer shelf life, early or late production, and varietal diversification. However, consumers are increasingly becoming aware of the potential benefits resulting from diets rich in fruits and vegetables for maintaining a good health and preventing diseases [1]. In this respect, the scientific literature provides a wealth of information that correlates a diet high in fruits and vegetables with better health and disease prevention [2,3]. This has stimulated a growing demand for vegetables with enhanced contents in bioactive compounds. Many bioactive molecules derived from vegetables are effective due to their antioxidant activity, which prevents the formation of reactive oxygen, nitrogen, hydroxyl and lipid species, by scavenging free radicals or by repairing or removing damaged molecules [4,5]. The most relevant antioxidant bioactive molecules found in fruits and vegetables generally include hydrosoluble vitamins, carotenoids, and phenolics [6,7,8]. Occasionally, other classes of molecules, like glucosinolates in the case of brassicas [9], have relevant bioactive properties that contribute to the functionality of fruits and vegetables.
Among the major groups of bioactive compounds of vegetables, phenolic acids (molecules containing a phenolic ring and an organic carboxylic acid function) are becoming the focus of attention of many researchers given their properties for human health and their relative abundance in vegetables (Table 1). Phenolic acids are one of the diverse classes of the many different phenolic compounds synthesized by plants and are commonly found in plant-derived foods [10,11,12]. The bioactive properties of phenolic acids from vegetables are numerous (see below in the section “Properties of phenolic acids”). This has resulted in an increasing interest in breeding for enhanced content in phenolic acids content in vegetables [13,14].
Increasing the content in phenolic acids content of vegetables can be achieved by a variety of means, including development of improved cultivars, use of specific cultivation conditions, and application of postharvest treatments [15]. In this review, we will focus on breeding new cultivars with improved content in phenolic acids. This will require identifying the phenolic acid compounds most important and abundant in vegetables, the search for sources of variation (including crop wild relatives) with potential as breeding materials, and discussion of breeding strategies and biotechnological approaches appropriated for developing new vegetable varieties with enhanced content in phenolic acids.
Table
Table 1. Average contents of total phenolic acids in different vegetables (mg/100 g of fresh weight) ranked according their average concentration (adapted from [12]).
Table 1. Average contents of total phenolic acids in different vegetables (mg/100 g of fresh weight) ranked according their average concentration (adapted from [12]).
VegetableTotal Phenolic Acids [mg/100 g fw]Major Soluble Phenolic Acids
Eggplant (Solanum melongena)32.0chlorogenic
Carrot (Daucus carota)29.5chlorogenic, caffeic, protocatechuic
Red beet (Beta vulgaris)27.0ferulic
Basil (Ocimum basilicum)22.0chlorogenic
Broccoli (Brassica oleracea var. italica)15.0sinapic, caffeic
Radish (Raphanus sativus var. sativus)12.0p-coumaric, ferulic
Spinach (Spinacia oleracea)11.0chlorogenic, protocatechuic, gallic
Chinese cabbage (Brassica pekinensis)7.7sinapic, chlorogenic
Parsley (Petroselinum crispum)6.2protocatechuic
Parsnip (Pastinaca sativa)5.7chlorogenic
Lettuce (Lactuca sativa var. capitata)5.1chlorogenic
Pepper (Capsicum annuum)4.7chlorogenic, p-coumaric, ferulic, protocatechuic
Cauliflower (Brassica oleracea var. botrytis)4.6p-coumaric, sinapic, chlorogenic
Turnip (Brassica rapa)4.6sinapic, ferulic, chlorogenic
White cabbage (Brassica oleracea var. capitata f. alba)3.8sinapic, p-coumaric
Grean bean (Phaseolus vulgaris)3.5chlorogenic, protocatechuic
Tomato (Solanum esculentum)3.5chlorogenic
Pea (Pisum sativum)1.3sinapic
Onion (Allium cepa)1.0protocatechuic, p-coumaric
Zucchini (Cucurbita pepo)0.9p-coumaric, caffeic
Cucumber (Cucumis sativus)0.1p-coumaric, ferulic

2. What Are Phenolic Acids?

Phenolic acids are secondary metabolites characterized by the presence of an aromatic ring with an organic carboxylic acid functionality. Phenolic acids derive from benzoic and cinnamic acids; and although their basic structure remains the same, the number of the hydroxyl groups and their positions on the aromatic ring vary greatly resulting in different phenolic acids [16,17,18]. The most commonly found phenolic acids derived from benzoic acid in vegetables include gallic, p-hydroxybenzoic, syringic and vanillic acids, while those derived from cinnamic acid include caffeic, chlorogenic, ferulic, p-coumaric and sinapic acids [18] (Figure 1). Generally, the concentration of the derivatives of cinnamic acid in fruits and vegetables is higher than that of benzoic acid, except for certain red fruits and other plant products [19]. In this respect, chlorogenic acid, which is caffeic acid esterified with quinic acid (Figure 2), is pre-eminent among phenolic acids in many vegetables [12]. Phenolic acids can be found in plant tissues either as in a free or, more frequently, in a bound form. The bound fraction is generally found as esters, glycosides or in complexes [20,21].
Molecules 20 18464 g001 550
Figure 1. Chemical structures of major cinnamic and benzoic acids derivatives found in vegetables.
Figure 1. Chemical structures of major cinnamic and benzoic acids derivatives found in vegetables.
Molecules 20 18464 g001
SubstitutionCinnamic Acid DerivativesBenzoic Acid Derivatives
R3 = OHp-Coumaric acidp-Hydroxybenzoic acid
R3 = R4 = OHCaffeic acidProtocatechuic acid
R2 = OCH3, R3 = OHFerulic acidVanillic acid
R2 = R3 = R4 = OHGallic acid
R2 = R4 = OCH3, R3= OHSinapic acidSyringic acid
R2 = R3 = OH [plus the carboxylic group being esterified with quinic acid]5-O-caffeoylquinic acid
Molecules 20 18464 g002 550
Figure 2. Structure of chlorogenic acid, a pre-eminent phenolic acid derivative present in many vegetables.
Figure 2. Structure of chlorogenic acid, a pre-eminent phenolic acid derivative present in many vegetables.
Molecules 20 18464 g002
Apart from their interest for human health, phenolic acids are very important for the quality of plant-based foods: they are substrates for enzymatic browning, and may affect flavour [22,23]. Furthermore, phenolic acids are signaling molecules involved in plant-microbe interactions [24].
Knowledge of the biochemical pathway of phenolic acid is important for molecular breeding strategies. Phenolic acids are biosynthetically formed through the shikimic acid pathway from l-phenylalanine or, to a lesser extent, from l-tyrosine [25]. The core pathway for the biosynthesis of phenolic acids involves the synthesis of cinnamic acid from L-phenylalanine catalyzed by phenylalanine ammonia-lyase (PAL) [26]. Cinnamic acid is then further transformed, through the catalytic action of different enzymes (e.g., hydroxylases, methytransferases), into many varieties of phenolic acids, catalyzed by (Figure 3). Benzoic acid is synthesized from cinnamic acid via the β-oxidative pathway [27]. Regarding derivatives of benzoic acid, hydroxylation and methylation processes are similar to those occurring for cinnamic acid derivatives, resulting in derived phenolic acids (Figure 3) [25,28].
Molecules 20 18464 g003 550
Figure 3. Schematic representation of some of the core biochemical pathways of major phenolic acids present in vegetables [25,29,30]. Enzymes involved in the pathways are indicated: PAL, phenylalanine ammonia lyase; C4H, cinnamate-4-hydroxylase; C3′H, p-coumarate 3′-hydroxylase; COMT, caffeic acid 3-O-methyltransferase; F5H, ferulate 5-hydroxylase; OMT, O-methyltransferase; 4CL 4-hydroxycinnamoyl-CoA-ligase; HCT, hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase; HQT, hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase; ECH, enoyl-CoA hydratase; ADH, cinnamoyl alcohol dehydrogenase; BA4H, benzoic acid 4-hydroxylase; PHBH, p-hydroxybenzoic acid 3-hydroxylase; PC5H, protocatechuic acid 5-hydroxylase.
Figure 3. Schematic representation of some of the core biochemical pathways of major phenolic acids present in vegetables [25,29,30]. Enzymes involved in the pathways are indicated: PAL, phenylalanine ammonia lyase; C4H, cinnamate-4-hydroxylase; C3′H, p-coumarate 3′-hydroxylase; COMT, caffeic acid 3-O-methyltransferase; F5H, ferulate 5-hydroxylase; OMT, O-methyltransferase; 4CL 4-hydroxycinnamoyl-CoA-ligase; HCT, hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase; HQT, hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase; ECH, enoyl-CoA hydratase; ADH, cinnamoyl alcohol dehydrogenase; BA4H, benzoic acid 4-hydroxylase; PHBH, p-hydroxybenzoic acid 3-hydroxylase; PC5H, protocatechuic acid 5-hydroxylase.
Molecules 20 18464 g003

3. Bioactive Properties of Phenolic Acids

Phenolic acids are powerful antioxidants as they act by donating hydrogen or electrons, which can delay or inhibit the oxidation of bio-molecules (DNA, proteins, and lipids) [7]. The high correlation coefficient between phenolic acids content and antioxidant capacity in vegetables reveals that they play a main role in the bioactive properties of these plant products [31]. The antioxidant capacity of the phenolic acids depends on its structure, and it is higher in molecules with large number of hydroxyls [5]. In this respect, in vitro antioxidant activities of phenolic acids are even much higher than those of other major antioxidants present in vegetables, like vitamin C, E, and β-carotene [32].
There are many studies showing that phenolic acids are beneficial for human health and have a main role in preventing chronic diseases and therefore an adequate intake of phenolic acids should be part of a healthy and equilibrated diet [10,21,33,34]. Many epidemiological studies have revealed biological activities beneficial for human health of phenolic acids present in vegetables such as cardioprotective, anticarcinogenic, antimicrobial, hepatoprotective, antianxiety, antidiabetic and antiobesity properties [21,35,36,37,38,39].

4. Breeding for Increased Phenolic Acids Content

Conventional breeding techniques, based on selection and hybridization, have shown a high potential for enhancing the content of bioactive compounds in a wide range of plants [40,41]. Genetic improvement of phenolic acids content can be accomplished by different techniques, like simple mass selection or individual selection of plants with desirable characteristics for seed or vegetative propagation, or through the deliberate crossing of closely or distantly related individuals in order to produce new crop varieties or hybrids with increased contents (Figure 4). Genetic variation is necessary for efficient and successful selection and breeding for increased phenolic acid contents, and usually most of their variation is quantitative rather than qualitative [42,43]. Therefore, in general the conventional selection and breeding methods to be used for enhancing the content in phenolic acids in vegetables will be those of quantitative traits.
Molecules 20 18464 g004 550
Figure 4. Summary of the main strategies for the development of new vegetable cultivars with increased content in phenolic acids. Screening and selection steps can be performed using phenotypic selection, marker assisted selection or both.
Figure 4. Summary of the main strategies for the development of new vegetable cultivars with increased content in phenolic acids. Screening and selection steps can be performed using phenotypic selection, marker assisted selection or both.
Molecules 20 18464 g004

4.1. Identification of Sources of Variation

Large variation has been found for phenolics acid content among samples of cultivated species [43,44,45,46,47,48,49,50,51,52]. Table 2 presents the variation found in different vegetables for chlorogenic acid content, revealing that large differences may exist within a single species for a given phenolic acid. This variation, which can be of several fold differences among accessions of the same species, can be exploited to select varieties with higher content in phenolic acids or to identify parental materials for breeding programmes (Figure 4).
Table
Table 2. Intraspecific variation for chlorogenic acid [g·kg−1 dw] content in different vegetables.
Table 2. Intraspecific variation for chlorogenic acid [g·kg−1 dw] content in different vegetables.
VegetableChlorogenic Acid [g·kg−1]References
Artichoke (Cynara scolymus L.)0.4–7.3[45]
Carrot (Daucus carota)0.3–18.8[46]
Chicory (Cichorium intybus L.)0.1–0.9[47]
Eggplant (Solanum melongena)1.4–28.0[48,49]
Lettuce (Lactuca sativa L.)0.1–0.3[50]
Pepper (Capsicum annuum)0.7–0.9[51]
Tomato (Solanum esculentum)0.2–0.4[52]
In some cases, morphological characteristics can provide an indication of the level of phenolic acids and therefore can be of interest for a preliminary selection of materials with potentially high content in phenolic acids. For example, Leja et al. [53] found that carrots with purple color roots possessed on average nine-fold higher phenolic acid content than carrots of other colors. Also, Vera-Guzmán et al. [54] reported that the color coordinates and chroma values presented a positive correlation with phenolic acid contents in Capsicum pepper. In the case of potato it was noticed that the pigmented cultivars like “Purple Majesty” and “Mountain Rose” contained considerably higher levels of chlorogenic acid isomers than the non-pigmented cultivars [55].
The origin may also be used on occasion for identification of sources of variation. For example, carrots of the Eastern (Asian) genepool often had higher content in phenolic acids than Western (European and American) genepool carrots [53]. Also, geographically-restricted Southeast Asian eggplants [S. melongena subsp. ovigerum] had a higher content in phenolic acids as well as greater diversity than eggplants from other regions [56].
Single mutations may represent an important source of variation for phenolic acid content (Figure 4). For example, mutants defective in light perception such as the high pigment [hp-1] mutant of tomato with increased fruit color result possess elevated chlorogenic acid content [57]. Also by utilizing somaclonal variation, a lettuce variety with high levels of chlorogenic acid was obtained [58].
Wild relatives are an important source of variability that can be used by plant breeders to develop vegetable varieties with increased contents in phenolic acids (Figure 4). For example, Meléndez-Martínez et al. [59] found that wild tomato species are a potential resource for increasing the phenolic acid content of tomato, as they presented higher concentrations than cultivated tomato. Also, in eggplant it has been found that artificial selection has resulted in a reduction in phenolic acids content and that wild relatives usually have higher contents in phenolic acids than cultivated eggplant [56]. In this crop, S. incanum, a wild relative of cultivated eggplant with high content in phenolic acids is being used in eggplant breeding programs as a source of variation for the introgression of this trait in the genetic background of eggplant by backcrossing [60,61]. Mennella et al. [62] studied the content in chlorogenic acid in lines of eggplant containing introgressions from three related species that had been selected for resistance to Fusarium and agronomic traits and found that S. sodomaeum introgression lines were highest in chlorogenic acid compared to introgression lines derived from two other species [S. integrifolium and S. aethiopicum]. Nonetheless, despite the interest of wild species as sources of variation for high content in phenolic acids, there are also associated disadvantages for breeding programmes, as they present many undesirable traits from the agronomic and commercial point of view [60,63,64]. As a result, selection against these traits has to be performed in the backcross generations. When traits to be removed are monogenic and dominant, selection will be much easier to be done than when are polygenic and with recessive inheritance.

4.2. Gene Action and Heritability

Knowledge of gene action and heritability values is important for devising efficient breeding strategies. However, there are few examples of determining these parameters for phenolic acids in vegetable crops. In a recent study by Prohens et al. [60], using a backcross population between cultivated eggplant and S. incanum, it was found that a simple additive-dominance model, in which only the additive variance was significant, explained the genetic variance for phenolic acid conjugate constituents. This indicates that genes from the wild species favoring the accumulation of phenolic acids should be in homozygosis in order to obtain higher contents in phenolic acids. Heritability studies for phenolic acid content of scarlet (S. aethiopicum) and gboma (S. macrocarpon) eggplants found moderate to high values of heritability for chlorogenic acid content and other phenolic acid contents and indicates that selection for these traits will be efficient in breeding programs [65].
The phenolic acid content is influenced by the growing environment and its interaction with the genotype [15,66,67]. For example, a recent study carried out by Stommel et al. [43] in order to evaluate the influence of the environment on fruit phenolics content in 12 different eggplant genotypes found a high genotype × environment interaction for phenolic acids content. However, these authors suggested that selection for stability could result in the selection of varieties with a reduced variability in phenolic acids content resulting from cultivation in different environments.

4.3. QTL and Candidate Genes for Phenolic Acids Content

New developments in molecular biology, genomics and metabolomics have provided new relevant information on the synthesis of phenolic acids. Detection and mapping of quantitative trait loci (QTL) in segregating populations or germplasm collections provides information of high interest for marker assisted selection and breeding [68]. Therefore, mapping major QTL for phenolic acids content will facilitate incorporation of this trait into élite vegetable cultivars through marker assisted selection.
Also, the candidate gene approach, which may be linked to the detection of QTLs, shows promise given that the genes involved in the phenolic acid synthesis pathway are known [Figure 3]. These genes are candidates for having a role in the accumulation of phenolic acids. In this respect, the genes codifying for enzymes involved in the core chlorogenic acid synthesis pathway in eggplant [PAL, C4H, 4CL, HCT, C3′H, HQT] were mapped on the eggplant genetic map, and it was shown that all of them, except for 4CL and HCT, were not linked, which may facilitate pyramiding of favorable alleles in a single variety [61]. The role of genes involved in the pathway of synthesis of phenolic acids on the accumulation of these compounds has been confirmed in some studies. For example, in tomato, the overexpression of the HQT gene increased the content in chlorogenic acid [30], while in potato it was found that the suppression of the expression of the HQT gene resulted in a reduction in the chlorogenic acid content of over 90% [69]. Other genes are also of interest for increasing the content in phenolic acids in vegetables. For example, in the case of tomato a major candidate gene associated to higher phenolic acid content expressing in fruit was identified as ERF1, which is a key gene in orchestrating the genes for phenolic content production in tomato [70]. In addition, the availability in Arabidopsis and other model plants of a large number of mutants of genes from the various branches of the phenylpropanoid pathway [71] may facilitate the identification in vegetables of candidate genes for increasing the content in phenolic acids.

5. Genetic Transformation for Increasing Phenolic Acids Content

Many transgenic strategies are available to enhance the nutritional value of crops; these strategies offer a rapid way to introduce desirable traits into elite verities [72], including the development of new cultivars with increased contents in phenolics (Figure 4). However, only a few studies in vegetables have been reported to increase phenolic acids content by using genetic transformation approach. For example, chlorogenic acid was increased up to 1.8-fold in tomato via constitutive expression of the hydroxycinnamoyltransferase HQT gene [30]. In an another recent study by Amaya et al. [73], the ectopic expression of the D-galacturonate reductase (FaGalUR) gene from strawberry aimed at increasing the ascorbic acid content led to a moderate increase in this antioxidant, but it simultaneously resulted in an increase of more than two-fold in chlorogenic acid content of tomato fruit. Also, the MYB family transcription factor AtMYB11 from Arabidopsis was noticed to be involved in the regulation of caffeoylquinic acid synthesis in tomato, as after transformation the transgenic plants had a significant increase in chlorogenic acid (18.1-fold) content compared to the non-transformed wild-type; also the contents of dicaffeoylquinic acids and tricaffeoylquinic acids were 68.0-fold and 108.4-fold higher in transgenic plants as compared to the wild-type. In the case of potato, constitutively expressed anti-sense strawberry chalcone synthase gene (CHS) resulted in a dramatic reduction of anthocyanin, flavonol and proanthocyanidines levels, while the phenylpropanoid pathway was upregulated leading to an increase in chlorogenic and caffeic acids contents [74].
Despite the potential of genetic transformation for increasing the content in phenolic acids in vegetables, the public acceptance of these genetically engineered crops is generally low [75]. In this respect, cisgenesis is a promising alternative to transgenesis for genetic engineering, with potentially less social rejection. Cisgenesis consists in the genetic transformation of a variety using only genetic material from the sexually compatible genepool [76]. In that case, it requires the identification of genes for phenolic acids from the sexually compatible genepool for introduction via genetic transformation.

6. Collateral Effects of Breeding for Phenolic Acids in Vegetables

Phenolic acids have relevant roles in plant life, including the response against biotic and abiotic stresses [77]. Apart from their bioactive properties for humans, phenolic acids have been associated with sensorial qualities of foods [78]. Additionally, the food industry has investigated the effects of phenolic acids on fruit maturation, enzymatic browning, and their roles as food preservatives [60,77]. In consequence, increasing phenolic acids content in vegetables may have an impact in other traits of interest, like tolerance to biotic and abiotic stress, browning, or flavor that should be taken into account in breeding new vegetable crops varieties.

6.1. Biotic and Abiotic Stresses

Phenolic acids are known to confer resistance to infection by a large number of pathogens, including fungi, bacteria, and viruses [79,80]. Increased synthesis of phenolic acids, which are incorporated to the cell wall of plants, takes place in response to biotic stress [81]. Phenolic acids are also known for their role in resistance to insect pests [82]. In this respect, resistance to thrips in chrysanthemum is attributed to higher chlorogenic and feruloyl quinic acid content [83]. Shivashankar et al. [84] found that resistance in chayote fruit against melon fly (Bactrocera cucurbitae) infestation was correlated with higher levels of p-coumaric acid. Nematoxic effects have also been reported for some acids like chlorogenic acid after nematode penetration [85]. It has also been demonstrated that phenolic acids may increase the tolerance to abiotic stresses. For example, salinity tolerance in lettuce is positively correlated with higher levels of chlorogenic acid [86]. In summary, the increase in the content in phenolic acids in vegetables may have a positive effect on resistance or tolerance to biotic and abiotic stresses. In this way, breeding for high content in bioactive phenolics in vegetables may lead to varieties more tolerant to stresses, which is an important objective in vegetable crops breeding.

6.2. Browning

Raising the total phenolic acids content may cause a negative effect on apparent quality of the fruit. In the case of vegetables when the tissue of interest is cut, phenolic acids, mostly stored in vacuoles, are oxidized resulting in brown coloration, i.e., enzymatic browning [22,87]. Enzymatic browning is mostly mediated by polyphenoloxidase enzymes. These oxidoreductases catalyze the hydroxylation of monophenols to diphenols. This reaction is comparatively slow and results in colorless products. Subsequently the same polyphenoloxidase enzymes catalyze the oxidation of diphenols to quinones, which is a fast reaction that yields brown colored products [88]. In consequence, a drawback of increasing the concentration of phenolic acids is that it may lead to a reduction in the apparent quality caused by the browning after exposure to the air [89]. However, it has been proposed that simultaneous selection for high content in phenolic acids combined with low activity PPO may result in a reduced or negligible impact on browning because of increased levels of phenolic acids in vegetables susceptible to enzymatic browning [61,90]. In this respect, it has been demonstrated, using transgenic approaches, that suppression of PPO activity results in a dramatic reduction of browning [91,92].

6.3. Flavour

Phenolic acids can contribute to the astringency and a have potential for causing bitterness in foods [93]. However, it has been found that phenolic acids, like chlorogenic acid, at the concentrations normally present in vegetables do not cause appreciable amount of bitterness [94], which is normally caused by other compounds like saponins, isocoumarins, glucosinolates and other compounds, like calcium, that may enhance bitterness [95,96,97]. In some cases, like in carrot, the content of isocoumarins increases with stress and can be responsible for the occasional bitter taste of carrots [96]. In the case, of phenolic acids, the cultivation environment may also have an important role in the phenolic acid levels [43], but it is unknown if this may have an effect on flavour of vegetables. Since literature is scarce on the effect of phenolic acids on flavour of vegetables further studies are needed to confirm the role of increased concentration of these acids on different flavour aspects of vegetables.

7. Future Prospects and Challenges

The development of vegetable crops with enhanced content in phenolic acids will benefit from the integration of conventional and modern techniques. In this respect, the germplasm collections of vegetable crops are largely unexplored regarding the content in phenolic acids and may allow the discovery of materials with high contents in phenolic acids [46,65,90]. Knowledge of candidate genes involved in the synthesis of phenolic acids [29,30,61] may also lead to the detection of new alleles in germplasm collections using EcoTILLING or sequencing techniques [98]. Also, the sequencing of genomes and the use of synteny among related species may be of great interest for the detection of genes and QTLs involved in phenolic acids accumulation in vegetable crops with limited genomic information [99]. Genome editing is also creating new opportunities for designing new varieties with increased content in phenolics through a non-transgenic approach [100,101]. With all the information already available and new developments, breeders have the challenge to develop a new generation of vegetables with enhanced bioactive properties resulting from an increased content in phenolic acids. These new varieties will have to be adapted to market requirements in terms of yield, shape, and organoleptic properties, which requires an integral breeding approach.

Acknowledgments

This research has been funded by Ministerio de Economía y Competividad and FEDER [grant AGL2012-34213]. Prashant Kaushik is thankful to Indian Council of Agricultural Research [ICAR] for providing an International Fellowship for doctoral studies. Isabel Andújar and Pietro Gramazio are grateful to Universitat Politècnica de València [Programa de Ayudas de Investigación y Desarrollo, PAID] for a postdoctoral and a predoctoral contract, respectively.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Boeing, H.; Bechthold, A.; Bub, A.; Ellinger, S.; Haller, D.; Kroke, A.; Leschik-Bonnet, E.; Müller, M.J.; Oberritter, H.; Schulze, M.; et al. Critical review: Vegetables and fruit in the prevention of chronic diseases. Eur. J. Nutr. 2012, 51, 637–663. [Google Scholar] [CrossRef] [PubMed]
  2. Lobo, V.; Patil, A.; Phatak, A.; Chandra, N. Free radicals, antioxidants, and functional foods: Impact on human health. Pharmacogn Rev. 2010, 4, 118–126. [Google Scholar] [CrossRef] [PubMed]
  3. Fulton, S.L.; McKinley, M.C.; Young, I.S.; Cardwell, C.R.; Woodside, J.V. The effect of increasing fruit and vegetable consumption on overall diet: A systematic review and meta-analysis. Crit. Rev. Food Sci. Nutr. 2014, in press. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Leopoldini, M.; Marino, T.; Russo, N.; Toscano, M. Antioxidant properties of phenolic compounds: H-atom versus electron transfer mechanism. J. Phys. Chem. A 2004, 108, 4916–4922. [Google Scholar] [CrossRef]
  5. Piazzon, A.; Vrhovsek, U.; Masuero, D.; Mattivi, F.; Mandoj, F.; Nardini, M. Antioxidant activity of phenolic acids and their metabolites: Synthesis and antioxidant properties of the sulfate derivatives of ferulic and caffeic acids and of the acyl glucuronide of ferulic acid. J. Agric. Food Chem. 2012, 60, 12312–12323. [Google Scholar] [CrossRef] [PubMed]
  6. Kaur, C.; Kapoor, H.C. Antioxidants in fruits and vegetables the millennium’s health. Int. J. Food Sci. Technol. 2001, 36, 703–725. [Google Scholar] [CrossRef]
  7. Gülçin, I. Antioxidant activity of food constituents-An overview. Arch. Toxicol. 2012, 86, 345–396. [Google Scholar] [CrossRef] [PubMed]
  8. Dasgupta, A.; Klein, K. Antioxidants in Food, Vitamins and Supplements; Elsevier Inc.: San Diego, CA, USA, 2014. [Google Scholar]
  9. Volden, J.; Borge, G.I.A.; Bengtsson, G.B.; Hansen, M.; Thygesen, I.E.; Wicklund, T. Effect of thermal treatment on glucosinolates and antioxidant related parameters in red cabbage (Brassica oleracea L ssp. capitata f. rubra). Food Chem. 2008, 109, 595–605. [Google Scholar] [CrossRef]
  10. Balasundram, N.; Sundram, K.; Samman, S. Phenolic compounds in plants and agri-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chem. 2006, 99, 191–203. [Google Scholar] [CrossRef]
  11. Herrmann, K.; Nagel, C.W. Occurrence and content of hydroxycinnamic and hydroxybenzoic acid compounds in foods. Crit. Rev. Food Sci. 1989, 28, 315–347. [Google Scholar] [CrossRef] [PubMed]
  12. Mattila, P.; Hellstrom, J. Phenolic acids in potatoes, vegetables, and some of their products. J. Food Compos. Anal. 2007, 20, 152–160. [Google Scholar] [CrossRef]
  13. Sands, D.C.; Morris, C.E.; Dratz, E.A.; Pilgeram, A. Elevating optimal human nutrition to a central goal of plant breeding and production of plant-based foods. Plant Sci. 2009, 177, 377–389. [Google Scholar] [CrossRef] [PubMed]
  14. Diamanti, J.; Battino, M.; Mezzetti, B. Breeding for fruit nutritional and nutraceutical quality. In Breeding for Fruit Quality; Jenks, M.A., Bebeli, J.P., Eds.; John Wiley & Sons: Hoboken, NJ, USA, 2011; pp. 61–80. [Google Scholar]
  15. Treutter, D. Managing Phenol Contents in Crop Plants by Phytochemical Farming and Breeding Visions and Constraints. Int. J. Mol. Sci. 2010, 11, 807–857. [Google Scholar] [PubMed]
  16. Stalikas, C.D. Extraction, Separation, and Detection Methods for Phenolic Acids and Flavonoids. J. Sep. Sci. 2007, 30, 3268–3295. [Google Scholar] [CrossRef] [PubMed]
  17. Quideau, S.; Deffieux, D.; Douat-Casassus, C.; Poységu, L. Plant polyphenols: Chemical properties, biological activities, and synthesis. Angew. Chem. Int. 2011, 50, 586–621. [Google Scholar] [CrossRef] [PubMed]
  18. Goleniowski, M.; Bonfill, M.; Cusido, R.; Palazón, J. Phenolic Acids. In Natural Products: Phytochemistry, Botany and Metabolism of Alkaloids, Phenolics and Terpenes; Ramawat, K.G., Mérillon, J.M., Eds.; Springer-Verlag: Berlin Heidelbergen, Germany, 2013; pp. 1951–1973. [Google Scholar]
  19. Mattila, P.; Hellstrom, J.; Torronen, R. Phenolic acids in berries, fruits and beverages. J. Agric. Food Chem. 2006, 54, 7193–7199. [Google Scholar] [CrossRef] [PubMed]
  20. Andjelkovic, M.; Camp, J.V.; Meulenaer, B.D.; Depaemelaere, G.; Socaciu, C.; Verloo, M.; Verhe, R. Iron-chelation properties of phenolic acids bearing catechol and galloyl groups. Food Chem. 2005, 98, 23–31. [Google Scholar] [CrossRef]
  21. El-Seedi, H.R.; El-Said, A.M.A.; Khalifa, S.A.M.; Goransson, F.L.U.; Bohlin, L.; Borg-Karlson, K.A.; Verpoorte, R. Biosynthesis, natural sources, dietary intake, pharmacokinetic properties, and biological activities of hydroxycinnamic acids. J. Agric. Food Chem. 2012, 60, 10877–10895. [Google Scholar] [CrossRef] [PubMed]
  22. Prohens, J.; Rodríguez-Burruezo, A.; Raigón, 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. [Google Scholar]
  23. Upadhyay, R.; Mohan Rao, L.J. An outlook on chlorogenic acids-occurrence, chemistry, technology, and biological activities. Crit. Rev. Food Sci. Nutr. 2013, 53, 968–984. [Google Scholar] [CrossRef] [PubMed]
  24. Mandal, S.M.; Chakraborty, D.; Dey, S. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav. 2010, 5, 359–368. [Google Scholar] [CrossRef] [PubMed]
  25. Heleno, A.S.; Martins, A.; Queiroz, P.R.J.M.; Ferreira, R.F.C.I. Bioactivity of phenolic acids: Metabolites versus parent compounds: A review. Food Chem. 2015, 173, 501–513. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Shahidi, F.; Naczk, M. Phenolics in Food and Nutraceuticals; CRC Press: Boca Raton, FL, USA, 2004; pp. 1–3. [Google Scholar]
  27. Qualley, A.V.; Wildham, J.R.; Adebesin, F.; Kish, C.M.; Dudareva, N. Completion of the core β-oxidative pathway of benzoic acid biosynthesis in plants. Proc. Natl. Acad. Sci. USA 2012, 109, 16383–16388. [Google Scholar] [CrossRef] [PubMed]
  28. Gross, G.G. Biosynthesis and metabolism of phenolic acids and monolignols. In Biosynthesis and Biodegradation of Wood Components; Higuchi, T., Ed.; Academic Press: Orlando, FL, USA, 1985; pp. 229–271. [Google Scholar]
  29. Comino, C.; Lanteri, S.; Portis, E.; Acquadro, A.; Romani, A.; Hehn, A.; Larbat, R.; Bourgaud, F. Isolation and functional characterization of a cDNA coding a hydroxycinnamoyltransferase involved in phenylpropanoid biosynthesis in Cynara cardunculus L. Plant Sci. 2010, 179, 338–347. [Google Scholar] [CrossRef] [PubMed]
  30. Niggeweg, R.; Michael, A.J.; Martin, C. Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 2004, 22, 746–754. [Google Scholar] [CrossRef] [PubMed]
  31. Stratil, P.; Klejdus, B.; Kuban, V. Determination of total content of phenolic compounds and their antioxidant activity in vegetables-evaluation of spectrophotometric methods. J. Agric. Food Chem. 2006, 54, 607–616. [Google Scholar] [CrossRef] [PubMed]
  32. Tsao, R.; Deng, Z. Separation procedures for naturally occurring antioxidant phytochemicals. J. Chromatogr. B 2004, 812, 85–99. [Google Scholar] [CrossRef]
  33. Nardini, M.; Natella, F.; Scaccini, C.; Ghiselli, A. Phenolic acids from beer are absorbed and extensively metabolized in humans. J. Nutr. Biochem. 2006, 17, 14–22. [Google Scholar] [CrossRef] [PubMed]
  34. Wittemer, S.M.; Ploch, M.; Windeck, T.; Muller, S.C.; Drewelow, B.; Derendorf, H.; Veit, M. Bioavailability and pharmacokinetics of caffeoylquinic acids and flavonoids after oral administration of artichoke leaf extracts in humans. Phytomedicine 2005, 12, 28–38. [Google Scholar] [CrossRef] [PubMed]
  35. Roche, A.; Ross, E.; Walsh, N.; O’Donnell, K.; Williams, A.; Klapp, M.; Fullard, N.; Edelstein, S. Representative literature on the phytonutrients category: Phenolic acids. Crit. Rev. Food Sci. Nutr. 2015. [Google Scholar] [CrossRef] [PubMed]
  36. Rahman, I.; Biswas, S.K.; Kirkham, P.A. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem. Pharmacol. 2006, 72, 1439–1452. [Google Scholar] [CrossRef] [PubMed]
  37. Cho, A.S.; Jeon, S.M.; Kim, M.J.; Yeo, J.; Seo, K.I.; Choi, M.S.; Lee, M.K. Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obesemice. Food Chem. Toxicol. 2010, 48, 937–943. [Google Scholar] [CrossRef] [PubMed]
  38. Sova, M. Antioxidant and antimicrobial activities of cinnamic acid derivatives. Mini-Rev. Med. Chem. 2012, 12, 749–767. [Google Scholar] [CrossRef] [PubMed]
  39. Manuja, R.; Sachdeva, S.; Jain, A.; Chaudhary, J. A comprehensive Review on Biological Activities of P-Hydroxy Benzoic Acid and Its Derivatives. Int. J. Pharm. Sci. Rev. Res. 2013, 22, 109–115. [Google Scholar]
  40. Balyan, H.S.; Gupta, P.K.; Kumar, S.; Dhariwal, R.; Jaiswal, V.; Tyagi, S.; Agarwal, P.; Gahlaut, V.; Kumari, S. Genetic improvement of grain protein content and other health-related constituents of wheat grain. Plant Breed. 2013, 132, 446–457. [Google Scholar] [CrossRef]
  41. Farneti, B.; Masuero, D.; Costa, F.; Magnago, P.; Malnoy, M.; Costa, G.; Vrhovsek, U.; Mattivi, F. Is there room for improving the nutraceutical composition of apple? J. Agric. Food Chem. 2015, 63, 2750–2759. [Google Scholar] [CrossRef] [PubMed]
  42. Parr, A.J.; Bolwell, G.P. Phenols in the plant and in man: The potential for possible nutritional enhancement of the diet by modifying the phenols content or profile. J. Sci. Food Agric. 2000, 80, 985–1012. [Google Scholar] [CrossRef]
  43. Stommel, R.J.; Whitaker, D.B.; Haynes, G.K.; Prohens, J. Genotype x environment interactions in eggplant for fruit phenolic acid content. Euphytica 2015, 205, 823–836. [Google Scholar] [CrossRef]
  44. Yao, Y.; Sang, W.; Zhou, M.J.; Ren, G.X. Phenolic composition and antioxidant activities of 11 celery cultivars. J. Food Sci. 2010, 75, 9–13. [Google Scholar] [CrossRef]
  45. Alarcón-Flores, I.M.; Romero-González, R.; Martinez Vidal, LJ.; Garrido Frenich, A. Determination of phenolic compounds in artichoke, garlic and spinach by Ultra-High-Performance Liquid Chromatography coupled to Tandem Mass Spectrometry. Food Anal. Methods 2014, 7, 2095–2106. [Google Scholar] [CrossRef]
  46. Sun, T.; Simon, P.W.; Tanumihardjo, S.A. Antioxidant phytochemicals and antioxidant capacity of biofortified carrots (Daucus carota L.) of various colors. J. Agric. Food Chem. 2009, 57, 4142–4147. [Google Scholar] [CrossRef] [PubMed]
  47. Sinkovic, L.; Demsar, L.; Znidarcic, D.; Vidrih, R.; Hribar, J.; Treutter, D. Phenolic profiles in leaves of chicory cultivars (Cichorium intybus L.) as influenced by organic and mineral fertilizers. Food Chem. 2015, 166, 507–513. [Google Scholar] [CrossRef] [PubMed]
  48. Luthria, D.L. A simplified UV spectral scan method for the estimation of phenolic acids and antioxidant capacity in eggplant pulp extracts. J. Funct. Foods 2012, 4, 238–242. [Google Scholar] [CrossRef]
  49. Mennella, G.; Lo Scalzo, R.; Fibiani, M.; D’Alessandro, A.; Francese, G.; Toppino, L.; Acciarri, N.; de Almeida, A.E.; Rotino, G.L. Chemical and bioactive quality traits during fruit ripening in eggplant (S. melongena L.) and allied species. J. Agric. Food Chem. 2012, 60, 11821–11831. [Google Scholar] [CrossRef] [PubMed]
  50. López, A.; Javier, G.A.; Fenoll, J.; Hellín, P.; Flores, P. Chemical composition and antioxidant capacity of lettuce: Comparative study of regular-sized (Romaine) and baby-sized (Little Gem and Mini Romaine) types. J. Food Compos. Anal. 2014, 33, 39–48. [Google Scholar] [CrossRef]
  51. Hallmann, E.; Rembiałkowska, E. Characterisation of antioxidant compounds in sweet bell pepper (Capsicum annuum L.) under organic and conventional growing systems. J. Sci. Food Agric. 2012, 92, 2409–2415. [Google Scholar] [CrossRef] [PubMed]
  52. Hallmann, E. The influence of organic and conventional cultivation systems on the nutritional value and content of bioactive compounds in selected tomato types. J. Sci. Food Agric. 2012, 92, 2840–2848. [Google Scholar] [CrossRef] [PubMed]
  53. Leja, M.; Kamińska, I.; Kramer, M.; Maksylewicz-Kaul, A.; Kammerer, D.; Carle, R.; Baranski, R. The content of phenolic compounds and radical scavenging activity varies with carrot origin and root color. Plant Foods Hum. Nutr. 2013, 68, 163–170. [Google Scholar] [CrossRef] [PubMed]
  54. Vera-Guzmán, M.A.; Chávez-Servia, L.J.; Carrillo-Rodríguez, C.J.; López, G.M. Phytochemical evaluation of wild and cultivated pepper (Capsicum annuum L. and C. pubescens Ruiz & Pav.) from Oaxaca, Mexico. Chilean J. Agric. Res. 2011, 71, 578–585. [Google Scholar]
  55. Stushnoff, C.; Holm, D.; Thomson, M.D.; Jiang, W.; Thomson, H.J.; Joyce, N.I.; Wilson, P. Antioxidant properties of cultivars and selections from the Colorado potato breeding program. Am. J. Potato. Res. 2008, 85, 267–276. [Google Scholar] [CrossRef]
  56. Meyer, S.R.; Whitaker, D.B.; Little, P.D.; Wu, B.S.; Kennelly, J.E.; Long, L.C.; Little, A. Parallel reductions in phenolic constituents resulting from the domestication of eggplant. Phytochemistry 2015, 115, 194–206. [Google Scholar] [CrossRef] [PubMed]
  57. Long, M.; Millar, D.J.; Kimura, Y.; Donovan, G.; Rees, J.; Fraser, P.D.; Bramley, P.M.; Bolwell, G.P. Metabolite profiling of carotenoid and phenolic pathways in carotenoid and transgenic pathways in mutant and transgenic lines of tomato: Identification of a high antioxidant fruit line. Phytochemistry 2006, 67, 1750–1757. [Google Scholar] [CrossRef] [PubMed]
  58. Cheng, M.D.; Pogrebnyak, N.; Kuhn, P.; Krueger, C.G.; Johnson, W.D.; Raskin, I. Development and phytochemical characterization of high polyphenol red lettuce with anti-diabetic properties. PLoS ONE 2014, 9, e91571. [Google Scholar] [CrossRef] [PubMed]
  59. Meléndez-Martínez, J.A.; Fraser, D.P.; Bramley, M.P. Accumulation of health promoting phytochemicals in wild relatives of tomato and their contribution to in vitro antioxidant activity. Phytochemistry 2010, 71, 1104–1114. [Google Scholar]
  60. Prohens, J.; Whitaker, D.B.; Plazas, M.; Vilanova, S.; Hurtado, M.; Blasco, M.; Gramazio, P.; Stommel, R.J. Genetic diversity in morphological characters and phenolic acids content resulting from an interspecific cross between eggplant, Solanum melongena, and its wild ancestor (S. incanum). Ann. Appl. Biol. 2013, 162, 242–257. [Google Scholar] [CrossRef]
  61. Gramazio, P.; Prohens, J.; Plazas, M.; Andújar, I.; Castillo, E.; Herraiz, F.J.; Knapp, S.; Meyer, S.R.; Vilanova, S. Location of the chlorogenic acid biosynthesis pathway and polyphenol oxidase genes in a new interspecific anchored linkage map of eggplant. BMC Plant. Biol. 2014, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Mennella, G.; Rotino, G.L.; Fibiani, M.; D’Alessandro, A.; Francese, G.; Toppino, L.; Cavallanti, F.; Acciarri, N.; Lo Scalzo, R. Characterization of health-related compounds in eggplant (Solanum melongena L.) lines derived from introgression of allied species. J. Agric. Food Chem. 2010, 58, 7597–7603. [Google Scholar] [CrossRef] [PubMed]
  63. Kalloo, G.; Chowdhury, J.B. Distant Hybridization of Crop Plants; Springer: Verlag Berlin, Heidelberg, Germany, 1992; Volume 16, p. 271. [Google Scholar]
  64. Hajjar, R.; Hodgkin, T. The use of wild relatives in crop improvement: A survey of developments over the last 20 years. Euphytica 2007, 156, 1–13. [Google Scholar] [CrossRef]
  65. Plazas, M.; Prohens, J.; Cuñat, N.A.; Vilanova, S.; Gramazio, P.; Herraiz, J.F.; Andújar, I. Reducing capacity, chlorogenic acid content and biological activity in a collection of scarlet (Solanum aethiopicum) and gboma (S. macrocarpon) eggplants. Int. J. Mol. Sci. 2014, 15, 17221–17241. [Google Scholar] [CrossRef] [PubMed]
  66. Pék, Z.; Daood, H.; Nagyné, M.G.; Neményi, A.; Helyes, L. Effect of environmental conditions and water status on the bioactive compounds of broccoli. Cent. Eur. J. Biol. 2013, 8, 777–787. [Google Scholar] [CrossRef]
  67. Helyes, L.; Lugasi, A.; Daood, H.G.; Pék, Z. The simultaneous effect of water supply and genotype on yield quantity, antioxidants content and composition of processing tomatoes. Not. Bot. Horti. Agrobo. 2014, 42, 143–149. [Google Scholar] [CrossRef]
  68. El-Soda, M.; Malosetti, M.; Zwaan, B.J.; Koornneef, M.; Aarts, M.G. Genotype × environment interaction QTL mapping in plants: Lessons from Arabidopsis. Trends Plant Sci. 2014, 19, 390–398. [Google Scholar] [CrossRef]
  69. Payyavula, S.R.; Shakya, R.; Sengoda, G.V.; Munyaneza, E.J.; Swamy, P.; Navarre, A.D. Synthesis and regulation of chlorogenic acid in potato: Rerouting phenylpropanoid flux in HQT-silenced lines. Plant. Biotechnol. J. 2015, 13, 551–564. [Google Scholar] [CrossRef]
  70. Di Matteo, A.; Ruggieri, V.; Sacco, A.; Rigano, M.M.; Carriero, F.; Bolger, A.; Fernie, A.R.; Frusciante, L.; Barone, A. Identification of candidate genes for phenolics accumulation in tomato fruit. Plant Sci. 2013, 205–206, 87–96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  71. Schoch, G.; Goepfert, S.; Morant, M.; Hehn, A.; Meyer, D.; Ullmann, P.; Werck-Reichhart, D. CYP98A3 from Arabidopsis thaliana is a 3-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 2001, 276, 36566–36574. [Google Scholar] [CrossRef] [PubMed]
  72. Zhu, C.; Naqvi, S.; Gomez-Galera, S.; Pelacho, A.M.; Capell, T.; Christou, P. Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci. 2007, 12, 548–555. [Google Scholar] [CrossRef] [PubMed]
  73. Amaya, I.; Osorio, S.; Martinez-Ferri, E.; Lima-Silva, V.; Doblas, G.V.; Fernández-Muñoz, R.; Fernie, R.A.; Botella, A.M.; Valpuesta, V. Increased antioxidant capacity in tomato by ectopic expression of the strawberry D-galacturonate reductase gene. Biotechnol. J. 2015, 10, 490–500. [Google Scholar] [CrossRef] [PubMed]
  74. Lukaszewicz, M.; Matysiak-Kata, I.; Skala, J. Antioxidant capacity manipulation in transgenic potato tuber by changes in phenolic content. J. Agric. Food Chem. 2004, 52, 1526–1533. [Google Scholar] [CrossRef] [PubMed]
  75. Nicolia, A.; Manzo, A.; Veronesi, F.; Rosellini, D. An overview of the last 10 years of genetically engineered crop safety research. Crit. Rev. Biotechnol. 2014, 34, 77–88. [Google Scholar] [CrossRef] [PubMed]
  76. Jacobsen, E.; Schouten, H.J. Cisgenesis strongly improves introgression breeding and induced translocation breeding of plants. Trends Biotechnol. 2007, 25, 219–223. [Google Scholar] [CrossRef] [PubMed]
  77. Robbins, R.J. Phenolic acids in foods: An overview of analytical methodology. J. Agric. Food Chem. 2003, 51, 2866–2887. [Google Scholar] [CrossRef] [PubMed]
  78. Tan, S.C. Determinants of eating quality in fruits and vegetables. Proc. Nutr. Soc. Aust. 2000, 24, 183–190. [Google Scholar]
  79. Dixon, A.R. Progress natural products and plant disease resistance. Nature 2001, 411, 843–847. [Google Scholar] [CrossRef]
  80. Singhai, K.P.; Sarma, K.B.; Srivastava, S.J. Phenolic acid content in potato peel determines natural infection of common scab caused by Streptomyces spp. World J. Microbiol. Biotechnol. 2011, 27, 1559–1567. [Google Scholar] [CrossRef]
  81. De Ascensao, A.R.; Dubery, I.A. Soluble and wall bound phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp. cubense. Phytochemistry 2003, 63, 679–686. [Google Scholar] [CrossRef]
  82. Ding, H.; Lamb, R.J.; Ames, N. Inducible production of phenolic acids in wheat and antibiotic resistance to Sitodiplosis mosellana. J. Chem. Ecol. 2000, 26, 969–985. [Google Scholar] [CrossRef]
  83. Leiss, K.A.; Maltese, F.; Choi, Y.H.; Verpoorte, R.; Klinkhamer, P.G. Identification of chlorogenic acid as a resistance factor for thrips in chrysanthemum. Plant Physiol. 2009, 150, 1567–1575. [Google Scholar] [CrossRef]
  84. Shivashankar, S.; Sumathi, M.; Krishnakumar, K.N.; Rao, K.V. Role of phenolic acids and enzymes of phenylpropanoid pathway in resistance of chayote fruit (Sechium edule) against infestation by melon fly (Bactrocera cucurbitae). Ann. Appl. Biol. 2015, 166, 420–433. [Google Scholar] [CrossRef]
  85. Chitwood, D.J. Phytochemical based strategies for nematode control. Annu. Rev. Phytopathol. 2002, 40, 221–249. [Google Scholar] [CrossRef] [PubMed]
  86. Mahmoudi, H.; Baatour, O.; Huang, J.; Nasri, N.; Salah, B.I.; Tarchoun, I.; Zaghdoudi, M.; Gruber, Y.M.; Lachaal, M.; Ouerghi, Z.; et al. Verte and Romaine lettuce varieties (Lactuca sativa L.) show differential responses to high NaCl concentrations. J. Plant Nutr. Soil Sci. 2012, 175, 641–648. [Google Scholar] [CrossRef]
  87. Lattanzio, V.; Cardinali, A.; di Venere, D.; Linsalata, V.; Palmeri, S. Browning phenomena in stored artichoke (Cynara scolymus L.) heads: Enzymic or chemical reactions? Food Chem. 1994, 50, 1–7. [Google Scholar] [CrossRef]
  88. Queiroz, C.; Lopes, M.L.M.; Fialho, E.; Valente-Mesquita, V.L. Polyphenol oxidase: Characteristics and mechanisms of browning control. Food Rev. Int. 2008, 24, 361–375. [Google Scholar] [CrossRef]
  89. Fruit Phenolics; Macheix, J.J.; Fleuriet, A.; Billot, J. (Eds.) CRC Press: Boca Raton, FL, USA, 1990; pp. 1–126.
  90. Plazas, M.; López-Gresa, M.P.; Vilanova, S.; Torres, C.; Hurtado, M.; Gramazio, P.; Andújar, I.; Herráiz, F.J.; Bellés, J.M.; Prohens, J. Diversity and relationships in key traits for functional and apparent quality in a collection of eggplant: Fruit phenolics content, antioxidant activity, polyphenol oxidase activity, and browning. J. Agric. Food Chem. 2013, 61, 8871–8879. [Google Scholar] [CrossRef] [PubMed]
  91. Murata, M.; Nishimura, M.; Murai, N.; Haruta, M.; Homma, S.; Itoh, Y. A transgenic apple callus showing reduced polyphenol oxidase activity and lower browning potential. Biosci. Biotechnol. Biochem. 2001, 65, 383–388. [Google Scholar] [CrossRef] [PubMed]
  92. Chi, M.; Bhagwat, B.; Lane, W.D.; Tang, G.L.; Su, Y.Q.; Sun, R.C.; Oomah, B.D.; Wiersma, P.A.; Xiang, Y. Reduced polyphenol oxidase gene expression and enzymatic browning in potato (Solanum tuberosum L.) with artificial microRNAs. BMC Plant Biol. 2014, 14, 62. [Google Scholar] [CrossRef] [PubMed]
  93. Buffo, R.A.; Cardelli-Freire, C. Coffee flavour: An overview. Flavour Frag. J. 2004, 19, 99–104. [Google Scholar] [CrossRef]
  94. Nagel, C.W.; Herrick, I.W.; Graber, W.R. Is chlorogenic acid bitter? J. Food Sci. 1987, 52, 213–213. [Google Scholar] [CrossRef]
  95. Dawid, C.; Hofmann, T. Quantitation and bitter taste contribution of saponins in fresh and cooked white asparagus (Asparagus officinalis L.). Food Chem. 2014, 145, 427–436. [Google Scholar] [CrossRef] [PubMed]
  96. Kreutzmann, S.; Christensen, L.P.; Edelenbos, M. Investigation of bitterness in carrots (Daucus carota L.) based on quantitative chemical and sensory analyses. LWT—Food Sci. Technol. 2008, 41, 193–205. [Google Scholar] [CrossRef]
  97. Tordoff, M.G.; Sandell, M.A. Vegetable bitterness is related to calcium content. Appetite 2009, 52, 498–504. [Google Scholar] [CrossRef] [PubMed]
  98. Barkley, N.A.; Wang, M.L. Application of TILLING and EcoTILLING as reverse genetic approaches to elucidate the function of genes in plants and animals. Curr. Genomics. 2008, 9, 212–226. [Google Scholar] [CrossRef] [PubMed]
  99. Morrell, P.L.; Buckler, E.S.; Ross-Ibarra, J. Crop genomics: Advances and applications. Nat. Rev. Genet. 2012, 13, 85–96. [Google Scholar] [CrossRef] [PubMed]
  100. Lozano-Juste, J.; Cutler, R.S. Plant genome engineering in full bloom. Trends Plant Sci. 2014, 19, 284–287. [Google Scholar] [CrossRef] [PubMed]
  101. Araki, M.; Ishii, T. Towards social acceptance of plant breeding by genome editing. Trends Plant Sci. 2015, 20, 145–149. [Google Scholar] [CrossRef] [PubMed]

Share and Cite

MDPI and ACS Style

Kaushik, P.; Andújar, I.; Vilanova, S.; Plazas, M.; Gramazio, P.; Herraiz, F.J.; Brar, N.S.; Prohens, J. Breeding Vegetables with Increased Content in Bioactive Phenolic Acids. Molecules 2015, 20, 18464-18481. https://doi.org/10.3390/molecules201018464

AMA Style

Kaushik P, Andújar I, Vilanova S, Plazas M, Gramazio P, Herraiz FJ, Brar NS, Prohens J. Breeding Vegetables with Increased Content in Bioactive Phenolic Acids. Molecules. 2015; 20(10):18464-18481. https://doi.org/10.3390/molecules201018464

Chicago/Turabian Style

Kaushik, Prashant, Isabel Andújar, Santiago Vilanova, Mariola Plazas, Pietro Gramazio, Francisco Javier Herraiz, Navjot Singh Brar, and Jaime Prohens. 2015. "Breeding Vegetables with Increased Content in Bioactive Phenolic Acids" Molecules 20, no. 10: 18464-18481. https://doi.org/10.3390/molecules201018464

APA Style

Kaushik, P., Andújar, I., Vilanova, S., Plazas, M., Gramazio, P., Herraiz, F. J., Brar, N. S., & Prohens, J. (2015). Breeding Vegetables with Increased Content in Bioactive Phenolic Acids. Molecules, 20(10), 18464-18481. https://doi.org/10.3390/molecules201018464

Article Metrics

Back to TopTop