Weighted grading types and scores.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
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He joined University of Veterinary and Animal Sciences during 2003 as Assistant Professor where he was later selected and appointed as Associate Professor and Professor, in 2006 and 2011 respectively. His research focus is on selection and breeding of large and small ruminants. He also supervises and evaluates postgraduate research to ensure successful and timely completion of the projects focusing on genetic improvement, enhancing breeding efficiency and production enhancement of farm animals. In addition, he participates and conducts trainings, workshops, conferences and seminars, and writes scientific publications to disseminate knowledge and techniques to the researchers and livestock producers about various areas of animal husbandry for improving behaviour, health, growth, fertility and production of livestock. 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[1] stated that in genomic analysis technologies, many new advancements promote the efficiency of plant breeding. They also determined that genome-wide association studies (GWAS) and genomic selection (GS) are very helpful, especially in various fruit tree breeding research programs. Breeding of fruit crops is not so easy, as it takes a very long time to get the quality fruits with good size of a tree, to overcome the juvenility period as well as to obtain desired fruits according to the aim of the breeding program [1]. Whole-genome sequences have been recently released for apple, peach, strawberry, Japanese apricot, and Chinese and European pear. After these developments, in breeding programs, marker-assisted selection has been used in wide genomics studies. These studies have caused to develop genome scale SNPs and SSR markers and to place reference linkage maps in Rosacea family to allow the identification of evolutionary relationships, which can be found in Genome Database in Rosaceae website. Yamamoto and Terakami [2] reviewed the recent advances in genomic studies and their practical applications for Rosaceae fruit trees, particularly in pear, apple, peach, and cherry.
Peach (Prunus persica [L.] Batsch) and nectarine (P. persica var. nectarine Maxim) belong to the Rosaceae family. Peach is widely cultivated due to its easy adaptability to different ecological conditions, early fruit set and a long period of harvest. Peach cultivation extends along 30–45° north and south parallels of latitude. At higher elevations, low winter temperatures and late spring frosts are limiting factors for peaches [3]. Around 21,638,953 tons of peaches are produced in an area of 1,538,174 ha across the world. Turkey ranks number 6, with a production of 637,573 tons/year in 29,092 ha area, following China (11,924,085 tons), Italy (1,401,795 tons), Spain (1,329,800 tons), the USA (964,890 tons), and Greece (666,200 tons) [4].
Fruit breeders preferred to work on peach breeding for its early fruiting habit and correlative characteristics [5]. In cultivar or rootstock breeding programs, disease tolerant genotypes, early or late ripening habit, improvement of fruit quality characteristics such as shape, aroma, flesh firmness, especially low chilling requirements and to improve tree shape were aimed [6]. Important characteristics on peach breeding have already been determined to be; white fruit flesh is dominant to yellow fruit flesh; pubescence to smooth skin; soft fruit flesh to firm and freestone to clingstone. In crossbreeding of peaches and nectarines, since pubescence characteristics are controlled by single gene, generally heterozygote variation of 3:1 is seen. In addition, several correlations between fruit flesh color and receptacle and the color of leaves are seen. These correlative characteristics reveal that early selection is available in peach breeding [7, 8].
Classical plant breeding depends on the phenotypic selection of superior genotypes obtained as a result of crossbreeding. However, genotype × environment interaction causes time consumption and is quite difficult. Moreover, phenotypic selection is expensive and most of the time is not feasible for some characteristics like tolerance to abiotic stress conditions. Marker-assisted selection is an approach developed as an alternative to these problems faced in classical plant breeding [9]. Usually, fruit demand of the consumers in peach is large weight and big-sized fruits, which are quantitative characters (QTLs) affected by several genes and various environmental conditions. Linge et al. [10] carried out an experiment on these characteristics and determined a genetic map of an F2 progeny with 117 individuals of PI91459 (‘NJ Weeping’) 9 ‘Bounty’ with SNP markers. The fruit quality characters such as fruit weight, height, width, and depth of the progeny and parents were determined in 2011 and in 2012 and were compared with SNP markers. They found a positive correlation between characteristics of fruit weight and characteristics of fruit size. They also constructed a SNP map obtained from 1148 markers distributed across more than eight linkage groups. With this study, they identified 28 QTLs for these characters in which 11 of them were stable in both2011 and 2012 [10].
Various regions of Turkey are suitable to grow peaches under different ecological conditions. The Marmara region can grow high chilling requiring peaches, but the ripening time of the latest peach cultivars is about mid-September. A peach breeding study was carried out by Eroglu [11] in this important peach growing area. In this project, five foreign cultivars (Rio Oso Gem, Fortuna, Monroe, Jungerman and Vivian) and four local types (Bayramiç Tüysüzü, Alyanak Hulu, Sarı Papa and Takunyacı I) were hybridized to obtain fresh market peaches and two foreign and one local type peaches were hybridized for processing peaches. Eroglu et al. [12] stated the fruit quality performances of 121 peach genotypes for fresh market and 35 genotypes for processing. Adana province in Cukurova plain at the Mediterranean region has a subtropical climate. It is located very close to the Mediterranean Sea, thus this condition is suitable to grow only low or midseason chilling requiring peach cultivars. Within 1 h distance to this area, in Taurus Mountains (1100 m elevation) region, high chilling requiring cultivars could be grown efficiently [5].
The first peach breeding study in Turkey was conducted by Tanriver and Kuden [13] on ‘Ustun’, a very late ripening (in mid-October) peach cultivar from the beginning of the 1990s. This study was carried out for [1] breeding of early cultivars for subtropical regions and [2] breeding of late ripening cultivars for cold regions, during 1995–1999. In the breeding experiments, carried out in Adana for early peach cultivars, Springtime, Suncrest, Flavorcrest and Redcap peach cultivars were used. Embryo rescue method was used with the combinations, where Springtime was used as a mother parent. As a result, embryo size was found to be important for the success of embryo rescue, and early cultivars should be used as pollinators. In the breeding studies to obtain late ripening peach cultivars, ‘Monroe’, ‘Rio-Oso-Gem’ and ‘Ustun’ were crossed reciprocally, while ‘J.H. Hale’ (pollen sterile) was used only as a mother plant at Pozantı Agricultural Research Center of Cukurova University. Seeds from crosses were grown in the orchards, of the Horticultural Department in Adana, under subtropical conditions. Morphological, pomological and isozyme analysis were also carried out in Adana [14].
Among the peach hybrids, especially Rio-Oso-Gem × Ustun combination yielded very good results, and six hybrids of this combination were placed among 20 promising candidate cultivars. As a result of this study, several high-quality, very late ripening hybrids were identified [15]. The best results for late ripening, yield and fruit quality characteristics were obtained from the hybrids of Rio-Oso-Gem × Ustun combination, Nos. 24 and 19. These were followed by Ustun × Monroe 14, J.H. Hale × Rio-Oso-Gem 14, Rio-Oso-Gem × Ustun 21, and Independence open pollinated hybrid No. 8. The promising genotypes were planted at the orchards of Pozanti Agricultural Research and Application Center to see the real performances of these high chilling requiring peach and nectarine genotypes. According to the observations among the hybrids, some of them were found to be resistant to Taphrina deformans. The band profiles of 12 enzyme systems of parent cultivars were investigated and polymorphism obtained in 7 enzyme systems (MDH, PRX, ADH, AMY, IDH, PEP and ACP). In 31 hybrids, polymorphism in enzyme systems was found to be suitable to Mendel Segregation rates. As a result of this experiment, two very late ripening peach cultivars from Rio Oso Gem × Ustun combination and two peach cultivars from J.H. Hale open pollination were registered and patented. All these new cultivars are of good quality and high chilling requiring cultivars.
The aim of the second peach breeding program was to improve some quality characteristics of Ustun peach to obtain high chilling, late ripening, good quality and good yielding peach, as well as nectarine cultivars. In this study, the pollen of Ustun cultivar was crossed with Venus and Stark Red Gold nectarines [16]. By crossing Venus and Stark Red Gold nectarines, with Ustun peach cultivar, 61 genotypes from VxU combination and 115 genotypes from SRGxU combination were obtained. A total of 176 genotypes were investigated for their morphological as well as phenological characteristics and were analyzed pomologically. Also, some pomological characters were compared by BPPCT009, MA014, MA040, and STS-OPAG8 SSR primer pairs to investigate the effectiveness of the marker-assisted selection in F1 genotypes.
In the weighted ranking method, VxU-55, VxU-41, VxU-34, VxU-14, VxU-1, VxU-13, VxU-24, VxU-26 peach genotypes and VxU-31, VxU-42, VxU-53, VxU-15 nectarine genotypes in VxU combination gave the highest points. In SRGxU combination, SRGxU-101, SRGxU-28, SRGxU-88, SRGxU-84, SRGxU-36, SRGxU-57, SRGxU-23, SRGxU-92, SRGxU-93 peach, and SRGxU-5 nectarine genotypes gave the highest points for the same scaling method.
No gene amplification was obtained from the PCR reactions among VxU and SRGxU populations analyzed by MA040 and STS-OPAG8 SSR primer pairs. BPPCT009 and MA014SSR primer pairs were also insufficient to determine fruit shape and free stone characteristics for VxU and SRGxU populations. These selected genotypes will eventually be taken under registration very soon.
Detailed information on this research is given below.
Another peach and apricot breeding program resistant to Sharka has been completed with a cooperative research between BETA Private Research Center, Malatya Fruit Research Institute and Cukurova University. This study aimed to obtain peach, nectarine, and apricot genotypes resistant to “Sharka” with crossbreeding method. Plum pox virus (PPV) causing Sharka disease is the most important viral agent for stone fruits. This disease is most harmful to apricot, plum, and peach trees. In Valencian Institute of Agricultural Research (IVIA), peach breeding program on apricot and on peach was started in 1993 and 1997, respectively. The aim of the study on apricot was to adapt to Southern Europe and to obtain high-quality cultivars resistant to the Sharka disease. Sharka or PPV is the most important limiting factor in the production of apricot. It was first described in Spain in 1984, causing serious loss of fruit and destruction of more than 1.5 million trees. The disease resistance breeding program is based on the transfer of resistance from local cultivars of Sharka disease to other cultivars by crossbreeding experiments. With 15 genotypes selected in accordance with the program’s objectives, they were worked on apricot production areas in Spain. The aim of the peach breeding program was to obtain new cultivars of peach and nectarine that ripen early and provide good quality cultivars found in the market. The main market in Spain is the European countries, just as the big world producers are in the countries. In some parts of Valencia, Murcia, and Andulacia, climatic conditions allow the production of early cultivars that mature so as not to conflict with other European countries. In this study, 15 apricot genotypes and 12 peach genotypes selected for the purposes of the peach breeding program have been defined as resistant to the Sharka disease [17].
The Sharka disease is a race such as PPV-D, PPV-M, and PPV-Rec, and new breeds can be taken out from a combination of these races. PPV-T is a combination of PPV-M and PPV-D races, and it was found to be a race belonging to Turkey. In this study, local apricot cultivars Hacıhaliloglu and Kabaası were crossed with foreign apricot cultivars such as Stark Early Orange, Rojo Pasion, Murciana, and P 1908 (peach clone from Prunus davidiana), which are known to be resistant to PPV. For peaches, commercial peach cultivars such as Flored and Carolina were crossed with PPV resistant Stark Early Orange (apricot) and P 1908 peach clone. In the hybridization studies, embryo rescue was performed with the combinations in which Flored peach variety was used as a mother parent, and in other combinations, the seeds were folded. Murashige & Skoog (MS) and Woody Plant Medium (WPM) nutrient media were used for embryo rescue combinations. Molecular studies were used to determine early resistance to Sharka disease in the hybridized individuals. Studies of the PGS1.21, PGS1.24, and ZP002 markers in hybrid subjects revealed the presence of resistance, tolerance, and susceptibility alleles. A total of 365 genotypes from crossing among 12 combinations of apricot and peach were tested with SSR markers (P GS1.21, PGS1.24, and ZP002). Approximately, 138 genotypes were found to be candidates for PPV resistance in future studies [18]. Individuals with endurance allele at the next stage of the study will be protected for other tests and observations to be made by grafting on the clone rootstock.
Current peach breeding work is focused on breeding of low chilling, good quality genotypes, and to obtain flat and nonacid peaches (Prunus persica var. platycarpa). For this aim, Venus, Maycrest, Early Silver, and Gransun peach and nectarine cultivars and four flat and nonacid local peach genotypes, which were obtained by a selection study (Flat peach genotype 1, Flat peach genotype 2, Flat peach genotype 4, and Flat peach genotype 5), were used as parents. Phenological observations (blistering, green tip, pink tip, balloon, full bloom, and fall of petals) and pomological analyses (fruit weight, fruit height, fruit length, fruit width, total acid, pH, firmness, fruit top color, ground color, fruit pulp color, freestone state, fruit shape, and pubesence) were also studied. Wang et al. [19] stated that the nonacid peaches are preferred in the market, and this trait is usually selected in the commercial breeding programs. A major gene (D/d) located on chromosome 5 of peach has been described for this character, where the nonacid character is determined by the dominant D allele. Flavor analysis in fruit juice samples taken from genotypes will be carried out using the HS-GCMS technique, while sugar and organic acids will be carried out by the HPLC technique. Thus, the aroma, sugar, and organic acid levels of each individual will be determined.
In this chapter, brief information on the results of the second (b) peach breeding experiment at Cukurova University is provided.
In this breeding study, Ustun peach cultivar was used as a father parent, and Venus and Stark Red Gold nectarine cultivars were used as mother parent. In the trial, 61 F1 hybrids obtained from Venus × Ustun crossbreeding and 115 F1 hybrids obtained from Stark Red Gold × Ustun crossbreeding, and a total of 176 F1 hybrids were used as plant material.
Ustun peach cultivar has been emerged as a result of bud mutation from peach cultivar of J.H.H. It matures between the first week and the third week of October (1400–1500 altitude). Fruit peel is fairly hairy, red cheek on yellow ground, fruit stalk is short, flesh is hard and yellow color and it has a very good aroma (Figure 1).
Ustun local peach cultivar.
Venus and Stark Red Gold are kinds of nectarine with a yellow flesh. They have quite good properties in terms of fruit weight, color, and taste. Venus matures 10 days later than the Stark Red Gold.
A total of 176 F1 hybrids, that is, 61 from Venus × Ustun crosses and 115 from Stark Red Gold × Ustun crosses were compared for their correlative, phenological (pink tip, balloon, first bloom, full bloom, harvest date), morphological (plant length and trunk diameter, tree form, flower property, flower color), and pomological (fruit weight, fruit height, fruit length, fruit width, seed weight, Brix, % acidity, pH, pulp/seed rate, fruit shape, fruit tip, rupture state of the fruit, pubesence, fruit top color, fruit ground color, red blush in flesh, fruit attractiveness, firmness, taste, freestone, and fruit flesh color) characteristics in this experiment [20, 21]. Also, the marker-assisted selection effectiveness of F1 peach hybrids was determined by two SSR markers.
High molecular weight genomic DNA was extracted from the leaf samples of each F1 hybrids for SSR analysis. SSR analysis was performed in accordance with Aka-Kacar et al. [22]. Two primer pairs (BPPCT009/b, MA014a) were used to generate the SSR genotyping. DNA profiles of parents and F1 hybrids were recorded, and their allelic profiles were compared. Results obtained from the SSR analysis were evaluated with the pomological features of genotypes.
If we consider the trunk diameter measurements on F1 hybrids, following results were obtained; In VxU combination, the highest value (87.65 mm) was obtained from VxU-18 genotype, whereas the lowest one (33.54 mm) was obtained from VxU-56 genotype. In SRGxU combination, the highest trunk diameter value (99.44 mm) was determined in SRGxU-9 genotype, while the lowest one (21.92 mm) was determined in SRGxU-100 genotype. The genotypes reached full bloom phase on March 11, the earliest and on April 6, the latest. The hybrids showed the characteristics of rosaceae and campanula flower [16].
To get faster growth and earlier fruit set, F1 seeds of the genotypes were sown and grown under the subtropical conditions of Adana at the Cukurova University (50 m elevation). The genotypes could not show their best performances in Adana, but they gave us early selection opportunities. Although to the low chilling and sea-level conditions in Adana, some genotypes showed very late ripening habit such as, September 3–18. If we consider Ustun late peach cultivar is ripening at the end of September in Pozanti, some of these genotypes could be ripen later than the parents under Pozanti conditions.
The highest mean fruit weights in VxU combination were obtained from VxU-58 (137.30 g) and VxU-55 (136.95 g) genotypes. In SRGxU combination, the highest fruit weights were obtained from SRGxU-32 (154.30 g) and SRGxU-82 (150.90 g) genotypes.
Brix values among all hybrids (Table 1) were the highest in VxU-4 (14.40), SRGxU-110 (13.0), and SRGxU-111 (13.0) genotypes. These results are in accordance with the results of Tanriver and Kuden [13] and Monet [7, 20, 23] who stated that the hybrids showed their best performances (fruit weight, color, Brix value, and especially for their harvesting dates) in the areas convenient for their chilling requirements. Harvesting dates and fruit characteristics of the selected genotypes are given in Tables 2 and 3.
Harvest date | 20 | Fruit shape | 7 |
Fruit weight | 20 | Fruit ground color | 7 |
Brix | 13 | Fruit tip state | 5 |
Attractiveness | 12 | Red color under skin | 3 |
Freestone state | 10 | Red color around seed | 3 |
Weighted grading types and scores.
Genotypes | Harvest date | Fruit weight (g) | TSS (%) | Acidity |
---|---|---|---|---|
VxU-55 | 08/14–27 | 136.95 | 12 | 0.73 |
VxU-41 | 08/27 | 173.20 | 12 | 0.68 |
VxU-34 | 08/26 | 163.10 | 15 | 0.64 |
VxU-14 | 08/26 | 171.28 | 12 | 0.68 |
VxU-1 | 07/12–21 | 108.60 | 12.9 | 0.75 |
VxU-13 | 08/20–27 | 120.12 | 13.15 | 0.82 |
VxU-24 | 08/1–13 | 142.25 | 11 | 0.54 |
VxU-26 | 08/14–09/18 | 129.15 | 12.9 | 0.66 |
VxU-31 | 09/03 | 79.8 | 13 | 0.77 |
VxU-42 | 08/02–09/03 | 108.23 | 11.5 | 0.51 |
VxU-53 | 06/28 | 131.74 | 10 | 1.03 |
VxU-15 | 06/10–29 | 87.42 | 10 | 0.60 |
SRGxU-101 | 08/14 | 161.75 | 12 | 0.53 |
SRGxU-28 | 07/24 | 109.8 | 12 | 0.50 |
SRGxU-88 | 08/14–27 | 136.95 | 12 | 0.48 |
SRGxU-84 | 07/04 | 164.21 | 12 | 0.67 |
SRGxU-36 | 08/12 | 152.89 | 10 | 0.38 |
SRGxU-57 | 07/27 | 106.6 | 10.5 | 0.66 |
SRGxU-23 | 07/23–08/27 | 118.37 | 11 | 0.69 |
SRGxU-92 | 07/12 | 110.64 | 10 | 0.58 |
SRGxU-93 | 07/08 | 209.17 | 12 | 0.46 |
SRGxU-5 | 08/24 | 108.09 | 11.5 | 0.49 |
Harvesting dates and the fruit characteristics of the selected genotypes.
Genotypes | Firmness (kg/cm2) | Freestone | Fruit shape | Pulp color | Pubescence |
---|---|---|---|---|---|
VxU-55 | 2.92 | Semi freestone | Oval | Yellow | Medium |
VxU-41 | 2.67 | Semi freestone | Round | Yellow | Medium |
VxU-34 | 2.19 | Cling stone | Round | Yellow | Medium |
VxU-14 | 2.06 | Cling stone | Round | Yellow | Medium |
VxU-1 | 3.12 | Freestone | Oval | Yellow | Medium |
VxU-13 | 1.88 | Cling stone | Oval | Yellow | Medium |
VxU-24 | 2.68 | Freestone | Oval | Yellow | Medium |
VxU-26 | 2.9 | Semi freestone | Oval | Yellow | Medium |
VxU-31 | 1.5 | Freestone | Oval | Yellow | Nectarine |
VxU-42 | 3.10 | Cling stone | Oval | Yellow | Nectarine |
VxU-53 | 3.06 | Cling stone | Oval | White-Red | Nectarine |
VxU-15 | 2.28 | Semi freestone | Round | White-Red | Nectarine |
SRGxU-101 | 2.07 | Freestone | Oval | Yellow | Medium |
SRGxU-28 | 3.26 | Freestone | Round | Yellow | Medium |
SRGxU-88 | 2.92 | Semi freestone | Oval | Yellow | Medium |
SRGxU-84 | 2.65 | Cling stone | Oval | Yellow | Medium |
SRGxU-36 | 1.86 | Freestone | Round | Yellow | Medium |
SRGxU-57 | 2.75 | Freestone | Round | Yellow | Medium |
SRGxU-23 | 2.45 | Freestone | Round | Yellow | Medium |
SRGxU-92 | 2.34 | Semi freestone | Oval | Yellow | Medium |
SRGxU-93 | 3.47 | Cling stone | Round | Yellow | Medium |
SRGxU-5 | 2.75 | Freestone | Round | Yellow | Nectarine |
The fruit characteristics of the selected genotypes.
The data obtained from the observations and analyzes were weighed out in the individuals in both combinations. According to results, VxU-55, VxU-41, VxU-34, VxU-14, VxU-1, Vx-13, VxU-24, and VxU-26 genotypes gave the best results among the peach genotypes in VxU combination. In the same combination, VxU-31, VxU-42, VxU-53, and VxU-15 were found to be the best nectarine genotypes. In the other combination (SRGxU), the performances were obtained from SRGxU-101, SRGxU-28, SRGxU-88, SRGxU-84, SRGxU-36, SRGxU-57, SRGxU-23, SRGxU-92, and SRGxU-93 peach genotypes and SRGxU-5 nectarine genotype (Table 1).
A total of 176 F1 hybrids were examined by using two different SSR primer pairs for early marker-assisted selection. The fruit characteristics of some F1 hybrids are found to be different as compared to their parents, while some of them were almost found to be the same.
Among the molecular data determined from MA014a primer pair, with pomological analysis of hybrids, more correct results were obtained from MA014a primer pair in the genotypes of SRGxU combination (42.02%) and in the genotypes of VxU combination (85.29%). Also, BPPCT009/b primer pair was used to determine freestone characteristics of the hybrids. SRGxU combination gave 38.35% of correct results, and VxU combination gave 30.50% of correct results. As a conclusion, for early selection criteria, SSR primer pairs are good molecular markers to be used for this aim. However, in this research, we could not obtain a very good relationship among our hybrids.
Dirlewanger et al. [24] stated that MA014a SSR primer pair is associated with fruit shape and flat fruit. In our experiments, we found that MA014a primer pair was more suitable to VxU population, but not for SRGxU population. For freestone character, BPPCT009/b SSR primer pair was used (Figure 2) to determine the freestone character. This primer was not compatible for SRGxU and VxU F1 populations. Freestone characters of hybrids and allelic profiles did not match each other properly. The photos of some of the selected genotypes are shown in Figures 3–16.
Polyacrylamide gel image of SSR bands of BPPCT009 primer pair with SRGxU population.
Fruits of VxU-55 genotype.
Fruits of VxU-41genotype.
Fruits of VxU-14 genotype.
Fruits of VxU-1 genotype.
Fruits of VxU-13 genotype.
Fruits of VxU-24 genotype.
Fruits of VxU-26 genotype.
Fruits of SRGxU-101 genotype.
Fruits of SRGxU-28 genotype.
Fruits of SRGxU-88 genotype.
Fruits of SRGxU-84 genotype.
Fruits of VxU-53 genotype.
Fruits of VxU-15 genotype.
Fruits of SRGxU-5 genotype.
This peach breeding study was carried out to obtain late ripening, high chilling, good quality peaches, and nectarines suitable for more continental climates. As a result of the experiment, some genotypes were found to be later fruit ripening producers than their parents (September 3–18) under Adana subtropical climatic conditions (23 m elevation). The results showed that these late genotypes could ripen later under the continental climatic conditions. This means that these genotypes could have better performances at Taurus Mountains in Pozanti under higher elevation conditions (1100 m).
One of the parents of these genotypes was Ustun, late peach cultivar, which ripened at the end of September in Pozanti. This observation lead us to think that some of these genotypes ripen on 3rd-18th September. Under Adana subtropical climatic conditions, they could ripen later than their parents in Pozantı (may be at the end of September or at the beginning of October). Thus, this will be a very good opportunity to get very high market prices with these very late season peaches and nectarines.
Considering the fruit quality characteristics of the genotypes, among F1 hybrids, VxU-18 and SRGxU-9 genotypes gave better trunk development than the others. For the fruit weight characteristics, SRGxU-32, SRGxU-82, VxU-58, and VxU-55 gave the biggest fruits among all the genotypes. The highest brix values were obtained from VxU-4, SRGxU-110, and SRGxU-111 genotypes.
In conclusion, the genotypes of VxU-55, VxU-41, VxU-34, VxU-14, VxU-1, Vx-13, VxU-24, VxU-26, SRGxU-101, SRGxU-28, SRGxU-88, SRGxU-84, SRGxU-36, SRGxU-57, SRGxU-23, SRGxU-92 and SRGxU-93 peaches and VxU-31, VxU-42, VxU-53, VxU-15 and SRGxU-5 nectarines were found to be promising ones.
The selected genotypes which were grafted onto GF-677 rootstock were taken to Pozanti Agricultural Research and Application Center at the Taurus Mountains in Pozanti to compare their performances at high chilling area under second selection. Also in the future studies, more locus specific molecular marker systems such as SSRs or SNPs could be used to find out better characterization of the hybrid populations.
In modern medicine and chiefly in the approach infectious diseases, nutrition seems to be a neglected or at least underestimated aspect, although it is recognised that it often plays an important role in the prevention of various diseases, including infectious ones [1, 2]. Flavonoids are abundant functional substances in plants with potential health benefits and are used as valuable food components or as supplements. Some of these substances may have an antiviral action or in any case be important in modulating the immune system and defending cells from the oxidative stress associated with infection.
\nFlavonoids are hydroxylated polyphenolic compounds based on the structure of the 15-carbon backbone of the parent flavone (2-phenyl-1,4-benzopyrone), which consists of two phenyl rings (A and B) and a heterocyclic ring (C) (Figure 1A). They can be divided into various classes based on their molecular structure and according to the C-ring replacements scheme: flavones, flavonols, isoflavones, anthocyanins, flavanols and flavanones. More than 4,000 varieties of flavonoids have been identified.
\nMolecular structure of flavone (A), quercetin (B), hesperetin (C) and hesperidin (D).
In the human diet, flavonols are widespread with quercetin standing out among them (Figure 1B). The most represented flavanone is hesperetin (Figure 1C) which is found in citrus fruits in glycosylated form as hesperidin (Figure 1D). Flavanones lack a double bond between C2 and C3 and this makes them chiral in the C2 position. Chirality implies that the B ring is not planar like in flavonols and is twisted with respect to the A-C rings. Such a difference in molecular orientation is relevant because it can affect the way the different flavonoids interact with their biological targets and therefore their bioactive properties.
\nQuercetin [International Union of Pure and Applied Chemistry (IUPAC) name: 2-(3,4-dihydroxyphenyl)-3,5,7-trihydroxychromen-4-one, with a molecular weight of 302.23 g/Mol] contains five hydroxyl groups linked in position 3,5,7,3′ and 4′ to the basic flavonol skeleton. In plants and as a consequence of biotransformation by the intestinal bacterial flora, some of these hydroxyl groups are glycosylated and constitute the main derivatives of quercetin. Hesperidin (with a molecular weight 610.6 g/Mol) is a glycosylated derivative of hesperetin [IUPAC name: (2S)-5,7-dihydroxy-2-(3-hydroxy-4-methoxyphenyl)-2,3-dihydrochromen-4-one, with a molecular weight of 302.28 g/Mol], with a 6-O-(alpha-L-rhamnopyranosyl) -beta-D-glucopyranosyl disaccharide in position 7 via a glycosidic bond.
\nThe structure–activity studies show that the antioxidant and anti-free radical properties of flavonoids are due to the ketone group, the double bond between the 2 and 3 carbons, the 3′, 4′-catechol and the 3-hydroxyl moiety in the flavonoid skeleton (the latter two are present in quercetin but not in hesperidin) [3]. The C2-C3 double bond extends the π conjugation to the carbonyl group in the C ring, so the radical elimination capacity of unsaturated flavonoids is greater than saturated structures, such as flavanones [4]. The antiradical capacity of flavonols in aqueous solvents is mainly exerted by the mechanism of electron transfer with sequential proton loss, associated with the C3 hydroxyl group, or of electron-proton transfer in the catechol component. Therefore, the type of substitution of the B ring is also considered as a determinant of the antiradical potency of flavonoids [4].
\nMany of the biological effects of flavonoids appear to be related to their ability to modulate receptors, enzymes, cell signalling cascades, rather than to a direct antioxidant effect. In fact, the maximum concentrations of flavonoids that can be reached in the blood with very high intakes (~ 2 μmol/L) are much lower than the concentrations of other antioxidants, such as ascorbic acid (~50 μmol/L) uric acid (200–400 μmol/L) and glutathione (700–1500 μmol/L). The functional interaction between flavonoids and enzymes or receptors occurs through hydrogen bonds and hydrophobic interactions with key amino acids of targeted proteins. For example, an inhibition of the activity of the enzyme xanthine oxidase by quercetin is exerted thanks to hydroxyl groups of C5 and C4 [5], and the anti-inflammatory activity depends not only on the number of free hydroxyl groups, but also on the methyl group [6]. Here the binding capacity of quercetin and hesperidin to some important proteins of the SARS-CoV-2 virus will be described in more detail.
\nIn fresh orange juice the hesperidin content represents about 30 mg per 100 ml [7], but it is found in greater quantities in the white part of the peel [8]. Quercetin is widely present in the plant kingdom [9, 10] with an average daily consumption of 25–50 milligrams [11], up to about 250 mg per day in “high-consumers” of fruit and vegetables [12].
\nBoth hesperidin and quercetin have long been known for their antioxidant, anti-inflammatory and anti-lipemic properties. This review will focus on their effects in viral infections, with special prominence on the recently exploded COVID-19 pandemic and its SARS-CoV-2 responsible virus. With the outbreak of COVID-19 and the scientific world’s focus on the search for preventive, antiviral and immunomodulatory substances, other particularly interesting characteristics of dietary phytochemicals have emerged. Many studies have highlighted the importance of the intracellular redox state as a new target for natural or synthetic drugs aimed at blocking both viral replication and excess inflammation [13, 14]. It has therefore been suggested that early flavonoid treatment may be a way to restore redox balance, prevent cell damage and the resulting inflammatory storm that causes lung damage with respiratory dysfunction [15, 16, 17, 18].
\nAlthough there is still no clinical evidence of efficacy for COVID-19, the two flavonoids are emerging as some of the most capable substances of specifically inhibiting binding to cellular receptors of the SARS-CoV-2 virus and its replication [8, 14, 19, 20, 21]. A recent randomised study, which appeared in as a preprint version, suggests that quercetin, administered together with vitamin C, could help health care workers in the prevention of SARS-CoV-2 infection [22].
\nHere we will examine the known mechanisms of action of hesperidin and quercetin, taking SARS-CoV-2 as a paradigm, and without neglecting to mention the important properties of these natural substances for health care in general. Following a logical order, the various passages of the disease will be dealt with starting from cellular infection to clinical consequences, specifying the points where these flavonoids could act.
\nTests on laboratory animals have shown the ability of flavonoids to inhibit infection by various viruses such as herpes simplex-1, parainfluenza and respiratory syncytial virus [23, 24], poliomyelitis-1 [25], rhinovirus [26, 27], hepatitis C [28], rotavirus [29], influenza [30, 31, 32, 33, 34, 35, 36], SARS-coronavirus-1 [37]. Here we will examine recent evidence regarding the SARS-CoV-2 virus in more detail.
\nCoronaviruses are a group of single-stranded RNA viruses with a corona-like morphology, mainly causing enteric and respiratory diseases of varying extents. Once the first mucosal barriers and possible intervention of the immune system have been overcome, the viruses enter the cell via specific receptors, the nucleic acid is then expressed causing various intracellular changes, including replication into multiple copies and various types of damage to the host cell. In each of these steps it is possible to imagine the action of compounds that tend to block entry or slow down replication and its pathological consequences (Figure 2).
\nIntracellular cycle of the SARS-CoV-2 virus. Green asterisks and numbers indicate the points of the flavonoid actions described in the text.
The internalisation of SARS-CoV-2 in human cells is mediated by the binding of the virus’ spike glycoprotein (S) to its receptor on cell membranes, which is the angiotensin converting enzyme 2 (ACE2) [38, 39]. ACE2 is expressed in many tissues including the lung, liver, heart, colon, oesophagus, intestine, kidney, and even the brain, which is consistent with the variety of cell types that can be infected, and the variety of symptoms reported in COVID-19 patients [40, 41, 42, 43, 44, 45]. The S protein has two subunits, the first of which contains a receptor binding domain (RBD), which is responsible for binding to ACE2. Binding and entry are also favoured by the presence of a polybasic cleavage site between the two subunits of the spike and by proteolytic enzymes attached to the receptor, of which trans membrane serine protease-2 (TMPRSS2) is particularly important.
\nThe discovery that the hesperidin molecule has a chemical–physical structure suitable for binding to the spike of the SARS-CoV-2 virus (* 1 in Figure 2) has recently aroused scientific interest [14, 46, 47, 48, 49, 50, 51]. Wu et al. [46] used in silico simulation techniques to screen 1066 natural substances with a potential antiviral effect, plus 78 antiviral drugs already known in the literature. Of all of them, hesperidin was the most suitable for binding to the SARS-CoV-2 spike, wedging into the shallow middle sulcus of the RBD, where some hydrophobic amino acids, including Tyr436, Try440, Leu442, Phe443, Phe476, Try475, Try481 and Tyr49 form a hydrophobic pocket to contain the compound.
\nVarious authors have confirmed the affinity of hesperidin for the RBD fragment of the spike protein and its ability to hinder the binding with ACE2 or to make the interaction unstable (Figure 3) [52, 53]. The anchoring of hesperidin is stabilised by two hydrogen bonds (shown with green lines in Figure 3) with the amino acids Phe457 and Glu455 on the spike protein. According to other in silico screening studies, hesperidin also has an affinity for TMPRSS2 protease, which is involved in the functioning of the receptor when the vesicle is internalised with the virus [54, 55].
\nBinding of the ACE2 protein with the spike in the presence of hesperidin. The RBD fragment of the spike protein (331–524) is shown in red, and the hesperidin molecule in the stick model and human ACE2 is shown in blue. Figure created using a diagram component from the cited work [52] with authorisation from Creative Commons.
Molecular dynamics simulations and energy landscape studies revealed that other flavonoids such as fisetin, quercetin and kaempferol bind to the ACE2-spike complex with favourable free energy [56]. Another group reported studies showing that quercetin has a high affinity for viral spikes, blocking the sites of interaction with cellular receptors [19]. According to other authors who followed a gene expression approach [57], quercetin is identifiable as one of the highest scoring natural substances, altering the expression of numerous human genes that encode SARS-CoV-2 protein targets, including ACE2.
\nA second theoretical site of flavonoid action is the main protease that allows the processing of the first proteins transferred from the viral genome (point *2 in Figure 1).
\nAfter interacting with membrane receptors and their associated proteases, the viral particle is internalised by means of a vesicle formed by the same membrane, the shell of which is then removed, allowing the release of the genomic RNA into the cytoplasm. The coding sequences of the genomic RNA are translated into pp1a and pp1ab proteins, which are then broken down by a proteolytic process for a total of 16 non-structural proteins. The main enzyme that carries out this transformation is called 3-chymotrypsin-like protease (3Clpro) or major protease (Mpro) by various authors and is in fact the target of many chemical antiviral drugs.
\nSome non-structural proteins then form a replication complex that uses genomic (+) RNA as a template. Eventually, the subgenomic RNAs produced through transcription are translated into structural proteins that will form new viral particles. For this purpose, structural proteins are incorporated into the membrane and the nucleocapsid N protein combines with the RNA produced through the replication process to become a nucleoprotein complex. The various components fuse into the complete viral particle in the Golgi endoplasmic reticulum apparatus, which is finally excreted in the extracellular region.
\nA strong affinity of hesperidin to Mpro has been discovered by various authors [46, 47, 50] in the screening of thousands of potential molecules using molecular docking techniques. Hesperidin binds with hydrogen bonds to various amino acids, mainly Thr24, Thr25, Thr45, His4, Ser46, Cys145 [50]. An important precedent exists when the authors investigated natural compounds capable of inhibiting Mpro of the SARS virus [37], using cell-based proteolytic cleavage assays. Out of seven phenolic compounds tested, hesperetin inhibited proteolytic activity efficiently with an IC50 of 8.3 μmol/L. Since the coronavirus main protease structure and active site conformation are preserved despite sequence variations [51], it is conceivable that the inhibitory effect of hesperidin, previously observed in the SARS virus, could also be exploited in SARS-CoV-2. Furthermore, hesperidin binds to structural protein 16 (nsp16) of the coronavirus, which is a methyltransferase dependent on S-adenosyl methionine [58]. This protein plays an important role in viral replication and prevents recognition by the innate immune system.
\nQuercetin has also been shown to inhibit the Mpro of the SARS-CoV [59], MERS-CoV [60] and SARS-CoV-2 [61] coronaviruses. The binding points of quercetin and hesperetin on SARS-CoV-2 Mpro are partially different [19]: the first in fact binds to Glu288, Asp289 and Glu290, while the second to Glu290, Asp289, Lys5. Furthermore, hesperetin, naringenin and kaempferol bind to the regulatory site Leu286, which quercetin does not do. All this suggests that the different molecules do not overlap as a pharmacological activity on the Mpro, but can synergise.
\nAn even more recent study [62] confirms the affinity of quercetin to Mpro using the measurement of the enzymatic activity. Evidence of its inhibitory effect was obtained with a fairly low dose of quercetin (7.7 μmol/L). Figure 4 shows the molecular complex formed by quercetin bound in the cavity that constitutes the active site of Mpro (in blue), in the most favourable position to inhibit the protein enzymatic activity in order to block the replication of the coronavirus.
\nRepresentation of the quercetin molecule (in orange) within the active site of the Mpro of the SARS-CoV-2 virus. Developed by Bruno Rizzuti on the basis of the study of which he is co-author [62]. Reproduction authorised by the author.
Da Silva et al. [63] have expanded the search for molecules interacting with Mpro to a series of flavonoid glycosides using a molecular docking approach. The interactions and binding affinity with the protease by quercetin and even more by its glycosidic derivatives quercetin-3-O-rutinoside (rutin), quercetin-3-O-glucuronide, quercetin-3′- O-sulphate, quercetin-7-O-glucuronide, quercetin-7-O-sulfate were thus predicted. It should be noted that the absorbed flavonoids normally undergo extensive metabolism in the epithelial cells of the small intestine and in the liver. Metabolites conjugated with the methyl, glucuronate and sulphate groups are the predominant forms present in plasma [64, 65, 66]. Quercetin has also been indicated as one of the substances capable of binding and thus inhibiting RNA-dependent RNA polymerase, an essential enzyme in the replication of viral RNA in the host cell [63].
\nRusso et al. [20] further confirmed the ability of known flavonoids (e.g. quercetin, baicalin, luteolin, hesperetin, gallocatechin gallate, epigallocatechin gallate) to inhibit the key proteins involved in the infectious cycle of SARS-CoV-2. They suggested that flavonoids and their derivatives, due to their pleiotropic activities and lack of systemic toxicity, may represent target compounds to be tested in future clinical trials to enrich the arsenal of drugs against coronavirus infections.
\nOxidative stress is an important cell pathology mechanism which is involved in many diseases, including those caused by viruses. Viral respiratory infections are generally associated with the production of cytokines, inflammation, cell death and other pathophysiological processes, which could be linked to increased production of reactive oxygen species (ROS), redox imbalance and oxidative stress.
\nMany lines of evidence suggest that viral infections are accompanied by signs of increased production of ROS, presence of oxidation products in blood plasma and urine, and reduced antioxidant capacity [67]. This pathological and pathogenic phenomenon has been observed in the infection of viruses such as hepatitis B [68], hepatitis C [69], influenza [70] and SARS-CoV-2 [71]. In the latter, ROS could also determine an unfavourable evolution in elderly subjects with low antioxidant capacity [72, 73], perhaps because the intracellular redox environment alters the presentation of antigens [74] and the expression of ACE2 [75, 76]. In fact, the severity and mortality risk of SARS-CoV-2 or COVID-19 have been associated with age [73].
\nStudies have shown that the ability of viral envelope glycoproteins to fuse to the surface of a cell membrane depends on the disulphide-thiol balance of the cell, even if the binding of coronaviruses to cell receptors seems rather insensitive to these parameters [77]. It seems possible that the oxidation of thiols to disulphides, under an oxidative stress mechanism, increases the affinity of spike proteins for the ACE2 receptor and, therefore, increases the severity of COVID-19 [75]. In this regard, reduced glutathione (GSH) may also have direct anti-SARS-CoV-2 potential: in fact, a computational study indicates that the binding of the spike protein to ACE2 is at its highest when the ACE2-sulfur groups are in the form of disulphides and are altered when they are fully reduced to thiols: therefore a pro-oxidant environment with low levels of GSH would favour the cellular entry of viruses [75, 78].
\nIn the course of viral diseases, analgesic and antipyretic drugs are widely used, and of these one of the most common is paracetamol (acetaminophen). However, the fact that this drug depletes glutathione reserves and can worsen oxidative stress is not always taken into account [78, 79]. This type of biochemical modifications can decrease the antiviral defences [80] or complicate the course especially in patients with abnormal liver tests or liver failure [81, 82].
\nAs described in the Introduction, flavonoids have a molecular structure capable of participating in redox reactions and free radical scavenging, which are involved in the biochemical phenomena described here and in the cellular pathology resulting from viral infection (point * 3 in Figure 2). Hesperidin contributes significantly to antioxidant defence systems and has been reported to act as an effective agent against superoxide and hydroxyl radicals [83], while hesperetin inhibits the production of nitric oxide by lipopolysaccharide (LPS)-stimulated microglial cells [84].
\nQuercetin also acts as a free radical scavenger, donating two electrons to oxidised species which are reduced. When this occurs with the transfer of one electron at a time, a semiquinonic intermediate molecule is formed. This antioxidant activity of quercetin is exploited in synergy with vitamin C, thanks to the ability of ascorbate to recycle the flavonol molecule, protecting it from oxidation and recycling its oxidised quinonic form after the scavenger action on free radicals [85]. In addition to ascorbic acid, glutathione is also important for maintaining quercetin in its reduced and therefore functional form and preventing the risk that quercetin quinone, in turn, may oxidise the thiol groups of proteins [86, 87].
\nVarious in vitro and in vivo studies have shown that the antioxidant activity of hesperidin and quercetin is not limited to their scavenger activity, but actually increases cellular defences against oxidative stress through the signalling path Nrf2/ARE [88, 89, 90, 91, 92, 93, 94, 95] (Figure 5).
\nOxidative stress induced by several pathogenic factors (top part) and cellular defensive effects of flavonoids, functioning as direct free radicals scavengers in synergy with ascorbate and other liposoluble vitamins (A, E) and as stimulants of the Nrf2/ARE pathway. O2-: Superoxide anion; H2O2: hydrogen peroxide; °OH: hydroxyl radical; LO2H: Lipid hydroperoxide; LPS: lipopolysaccharide; Keap1: Kelch-like ECH-associated protein 1; Nrf2: nuclear factor erythroid 2–related factor 2; Maf: musculoaponeurotic fibrosarcoma element; ARE: antioxidant response element.
The nuclear factor erythroid 2–related factor 2 (Nrf2) is of primary importance because it regulates gene expression through a promoter sequence known as the antioxidant response element (ARE). Normally Nrf2 is attached to another protein called Kelch-like ECH-associated protein 1 (Keap1) and is rapidly degraded through the ubiquitination and proteasome system, without performing any functions. On the other hand, in the presence of ROS, Nrf2 detaches from Keap1, is phosphorylated and translocates to the nucleus, where it combines with a small musculoaponeurotic fibrosarcoma (Maf) protein to form a dimer and binds to the antioxidant response element upstream of the promoter. This ARE + Nrf2 dimer then initiates the messenger RNA transcription of a series of target genes such as those encoding antioxidant enzymes (“Antioxidant systems” in Figure 5).
\nThe ability of hesperidin to fight damage from toxic oxygen radicals and stimulate the expression of Nrf2 has been reported by various authors in other experimental models namely in hepatocarcinogenesis [96], hepatotoxicity [97], neuroinflammation and neurodegeneration [91, 98, 99, 100, 101, 102]. The protective effects of quercetin in neurodegenerative disorders and cerebrovascular diseases, demonstrated both in in vitro and in vivo studies are also largely linked to its ability to stimulate the defences against oxidative stress [103].
\nOnce they have reproduced in the cells of the entry tissues and overcome the first barriers of innate defences, the viruses spread to target organs and cause various types of clinical consequences in different individuals. It is known that the severity of COVID-19 as well as other viral respiratory infections is related to many different parameters (age, gender, nutritional status, comorbidities, etc.) and that people with pre-existing conditions such as diabetes, hypertension, and lung, heart and kidney diseases (all diseases in which ROS play a pathogenetic role) are at increased risk of developing severe effects. In serious cases, endothelial dysfunction, coagulopathy and pulmonary thrombosis cause hypoxia, mitochondrial chain abnormalities, mitochondrial dysfunction, oxidative stress, DNA damage [104, 105]. Another mechanism that links systemic inflammation syndrome and oxidative stress is hyperferritinemia, which often characterises COVID-19 [106, 107].
\nThese mechanisms are involved in the extensive systemic lesions observed during severe complications associated with influenza. It has therefore been suggested that agents with antioxidant properties could be drugs of choice for the treatment of patients with such severe complications [108]. N-acetylcysteine, which supports glutathione and thus the main antioxidant defence systems [109], was used with good results in influenza syndromes [110] and acute respiratory distress syndrome (ARDS) [111], and it was suggested as a potential therapeutic agent for COVID-19 [112, 113, 114].
\n\nFigure 6 summarises the main critical points of the SARS-CoV-2 virus in the whole body and the possible interventions of the two flavonoids considered here, based on the knowledge acquired so far in other types of systemic and metabolic disorders.
\nDiagram of the major systemic effects of COVID-19. The asterisks show the possible operation points of the flavonoids, as discussed in chapter 2 (*1, *2, *3) and in this chapter (*3, *4 and *5).
Experimental evidence showed that treatment with hesperidin safeguards the aged rat’s heart by increasing the levels of the Nrf2 factor and the activity of enzymatic antioxidants [115]. The same group showed a protective effect of hesperetin on experimental heart failure in the rat [116]. The authors conclude that it is conceivable that hesperetin could be a potential therapeutic candidate that enhances Nrf2 signalling and thereby improves cardiac remodelling. Results from another study show the beneficial effects of citrus flavanones in the liver of aged rats, where nirangerin and hesperidin prevented the age-related decrease in catalase, superoxide dismutase and glutathione reductase [117].
\nThe mechanism of ischemia–reperfusion liver injury was studied in a murine model by measuring oxidative stress indicators, serum enzymes and inflammation indices [118]. Hesperidin (100–400 mg/kg) significantly improved liver ischemia–reperfusion injury measured by serum alanine aminotransferase levels, reduced malondialdehyde content, but it increased superoxide dismutase, catalase, glutathione peroxidase levels. Furthermore, hesperidin significantly alleviated the expression levels of TNF-α, IL 6 and IL-1β. Hesperidin (100 mg/kg) protects rats from liver damage and dyslipidaemia caused by cadmium chloride [119].
\nThe antioxidant effect of quercetin was studied in a two-week, randomised, crossover-controlled intervention trial [120]. Fourteen individuals ingested 2 capsules (total 1 g/d) of quercetin or a placebo. Blood samples were collected before, after 2 weeks of supplementation and after a period of strenuous exercise. Quercetin significantly reduced erythrocyte lipid peroxidation levels and susceptibility to haemolysis induced by free radicals, while no differences were found in antioxidant enzyme activities and glutathione homeostasis between the two groups. After a single period of intense exercise, quercetin supplementation improved redox status as assessed by the reduced glutathione/oxidised glutathione ratio and by thiobarbituric acid reactive substances levels in both erythrocytes and plasma.
\nDuring the spread of the virus in the tissues (first of all in the lung) and systemically (lymph, blood, immune system, coagulation, kidney, liver), an inflammatory reaction develops which can be clinically very serious, especially in patients with comorbidities. Excessive and “vicious” inflammation can be mediated by a distorted activation of the cytokine network, by coagulation disorders, even by a paradoxical excess of the immune reaction (autoimmunity, cytotoxic lymphocytes) [121]. Oxidative stress and excess inflammation are linked, as shown in Figure 6 (points *3 e *4). Autoimmune phenomena are also likely to be involved in the attack on the cell infected with SARS-CoV-2, which could have implications both in the clinical course of the disease [122, 123] and in the safety of vaccines [124].
\nThe two flavonoids which are reviewed here have a remarkable ability to modulate local and systemic inflammatory responses, through various mechanisms. Hesperidin showed antioxidant activity in rats after an intense training programme and, at the same time, alleviated cytokine secretion by stimulated macrophages [125, 126]. Furthermore, the administration of hesperetin has been shown to significantly reduce the levels of myeloperoxidase, malondialdehyde (a marker of lipid peroxidation) and inflammation in experimental models of colitis [127] and hepatic trauma [128]. A study on macrophage cells in culture induced by bacterial endotoxin (LPS) clearly highlighted the main molecular effects of hesperetin capable of modulating inflammation [129].
\nOne of the most frequently used experimental models is LPS-induced pneumonia in mice, which somewhat mimics ARDS. Three separate studies have shown that hesperidin (in doses between 10 and 200 mg/kg) significantly reduces the accumulation of fluid in the lung and proinflammatory cytokines [130, 131, 132]. The protective and anti-inflammatory effect of hesperidin or hesperetin was also demonstrated in rats with acute lung injury induced by mechanical ventilation [133] and lung infection with the H1N1 influenza virus [36]. Finally, hesperidin has anti-inflammatory and antioxidant effects in chronic obstructive pulmonary disease (COPD) caused by smoking, reducing the levels of IL-6, IL-8 and malondialdehyde [134].
\nQuercetin is a powerful antioxidant but also acts as an enzymatic inhibitor in a series of mechanisms involved with inflammation [135]. In LPS-stimulated macrophages, quercetin treatment inhibited NF-kB activation and proinflammatory cytokines [136]. A randomised, parallel-group, controlled polycentric study showed the efficacy of a dietary supplement based on quercetin (150 mg), perilla dry extract (80 mg) and vitamin D3 (5 μg) in preventing allergic rhinitis flare-ups in children [137, 138].
\nThe antiallergic property of quercetin has been explored in the laboratory setting by studying the secretory response of activated mast cells in both human and animal models [139, 140, 141, 142, 143], and by evaluating the release of histamine from human basophils [144, 145]. This flavonol inhibits several protein tyrosine and serine/threonine kinases involved in signal transduction in inflammatory cells [26, 103, 139, 146, 147, 148]. These inhibitory properties on the release of histamine could also be interesting for COVID-19, given that the pulmonary mast cells are involved in the phenomenon of worsening the pulmonary picture in the event of a “cytokine storm” [149].
\nA meta-analysis of seven randomised trials sought to quantify the effect of quercetin on inflammatory mechanisms in vivo by measuring plasma C-reactive protein (CRP) concentrations. Meta-analysis showed a significant reduction in circulating CRP levels following supplementation with quercetin, especially at doses of 500 mg /day or more and in patients with CRP <3 mg/l [150].
\nSince COVID-19 is a multi-organ disease and has more serious clinical consequences in patients with pulmonary, intestinal, hepatic and cardiovascular comorbidities, it is conceivable that its clinical course may profit from the multiple beneficial effects of hesperidin and quercetin in systemic pathologies of this type (point * 5 in Figure 6). Epidemiological studies have reported an inverse relationship between citrus flavonoid intake and the risk of cardiovascular disease [151, 152]. From a careful review of the literature [153], the use of natural antioxidant polyphenols seems to be an excellent approach as they have strong antioxidant and anti-inflammatory properties.
\nA constellation of risk factors for cardiovascular disease is called metabolic syndrome (MetS), whose determining factors are, in order of importance: weight, genetics, ageing and lifestyle [154]. The criteria for defining MetS are based on the presence of 3 out of 5 factors, including obesity, elevated triglycerides, reduced HDL-C, elevated blood pressure and elevated fasting glucose [155]. It has been shown that individuals with these characteristics are also commonly prone to a chronic, low-grade inflammatory states. Oxidative stress phenomena are also involved in MetS, probably due to the disturbance of the nutrient metabolism at the mitochondrial level [154].
\nIn this context, it is interesting to note that good results have been obtained in clinical studies with the integration of orange juice, polyphenols and particularly with both hesperidin and quercetin, with antioxidant and antihypertensive effects, and by regulating glucose metabolism and lipid profiles. A recent experimental study showed that hesperidin (15 or 30 mg/kg) improved biochemical alterations and cardiac dysfunction in a high-fat diet-induced MetS model in rats [156].
\nSoy isoflavones, citrus products, hesperidin and quercetin improved lipid metabolism [157]. Rizza et al. [158] performed a randomised, placebo-controlled study to investigate whether oral administration of hesperidin (500 mg once daily for 3 weeks) improves endothelial function in individuals with MetS. As a measure of efficacy, they measured the difference in flow-mediated dilation of the brachial artery between subjects receiving placebo or hesperidin. In the clinical study, hesperidin treatment increased flow-mediated dilation and decreased the circulating inflammatory biomarkers (highly sensitive C-reactive protein, serum amyloid A protein, soluble E-selectin). The authors concluded that hesperidin recovers endothelial dysfunction and reduces circulating markers of inflammation. Such vasculoprotective actions may explain the beneficial cardiovascular effects of citrus fruit consumption.
\nA double-blind study documented the beneficial effects of hesperidin supplementation (500 mg/day) on blood pressure and inflammatory markers in type 2 diabetes [159]. The mechanisms by which hesperidin could contribute to blood pressure control are associated with improvements in endothelial function, oxidative stress and inflammation [160]. In a study with a parallel group design, 49 patients with MetS received either 500 mg of hesperidin or a placebo, twice daily for 12 weeks [155]. Hesperidin led to a significant decrease in serum levels of glucose, insulin, triglycerides, total cholesterol, low density lipoprotein cholesterol, TNF-α and high sensitive-CRP. The data on the antihypertensive effect of hesperidin is more uncertain but recently Valls et al. published a study on healthy volunteers in which they actually showed an antihypertensive effect of orange juice enriched with hesperidin [152].
\nA systematic review has highlighted the potential antidiabetic action of citrus flavonoids and their molecular mechanisms based on in vitro and in vivo studies [161]. The research identified 38 articles, mostly on experimental animals, which reported that citrus flavonoids regulate glycaemic control biomarkers, lipid profiles, kidney function, liver enzymes and antioxidant enzymes, and modulated signalling pathways related to glucose uptake and insulin sensitivity that are involved in the pathogenesis of diabetes and its related complications. Citrus flavonoids, therefore, are promising antidiabetic candidates, while their antidiabetic effects have yet to be verified in upcoming human studies.
\nQuercetin supplementation also may have positive effects among patients with MetS and related disorders [162]. A meta-analysis identified 9 studies on this topic, which showed overall that quercetin supplementation did not affect fasting plasma glucose or insulin resistance. However, in the subgroup analysis, quercetin supplementation slightly but significantly reduced fasting glucose in studies lasting 8 weeks and using quercetin in doses equal to or > 500 mg/day. Better effects were found in individuals <45 years of age. Regarding lipid levels, a meta-analysis of 9 clinical studies [163] found a significant reduction in LDL in overweight and obese human subjects who took doses ≥250 mg/day of quercetin for rather extended periods, reaching a total dose of ≥14,000 mg; however, HDL cholesterol, triglyceride and total cholesterol levels remained unchanged (p > 0.05).
\nThe supplementation of nutrition with quercetin on blood pressure and endothelial function among patients with MetS was investigated with a meta-analysis [164]. The authors found a significant reduction in systolic blood pressure but not diastolic pressure.
\nFinally, the health of the intestine cannot be neglected, which is an organ where viral infections tend to be found, and it is also fundamental because the release of endotoxins (LPS) due to an increased mucosa permeability or intestinal dysmicrobism could enhance systemic inflammatory reactions. It has been argued that the interaction between the lung and gut could lead to a vicious cycle of lung and intestinal inflammation which may be a potential factor leading to the death of patients with COVID-19 [165]. Citrus flavanones may have an impact on the intestinal microbiome, exerting beneficial effects on the intestinal barrier function and gastrointestinal inflammation [166]. In intervention studies on volunteers, orange juice positively modulated the composition and metabolic activity of the microbiota, increasing the population of Bifidobacterium spp. and Lactobacillus spp. [167] or of Lactobacillus spp., Akkermansia spp. and Ruminococcus spp. according to other authors [168], suggesting that orange juice showed a prebiotic effect, modulating the intestinal microbiota by improving blood sugar and the lipid profile. In a recent review [169], it was highlighted how the beneficial effects of hesperidin on cardiovascular risk factors can be partly attributed to the modulation of the intestinal microbiota. Based on the current evidence, some of the contradictory effects of hesperidin in human studies are in part due to the interindividual variability of hesperidin in its bioavailability. Quercetin also has a profound influence on the intestinal microbiome, which in turn modulates its bioavailability [170].
\nIn conclusion, the results indicate that supplementation with hesperidin or quercetin may have mild antihypertensive effects, improve metabolic lipid abnormalities and inflammatory status in patients with MetS. All these beneficial effects can only be reflected in a more favourable clinical course when viral infectious diseases cause systemic disorders involving oxidative stress and inflammation.
\nThe scientific literature is filled with works that support the beneficial effects of citrus flavonoids and quercetin on viral respiratory diseases, including COVID-19, and there are several possible mechanisms by which this effect is carried out (Figure 7).
\nSummary of the possible actions of flavonoids hesperidin and quercetin to prevent the progression of SARS-CoV-2 virus infection and its major clinical consequences.
Inhibition of cellular infection can occur through the intercalation of these molecules between viruses and receptors and by inhibition of intracellular replication. This phenomenon could have a protective role especially in the oral cavity and in the gastrointestinal system, where the concentrations of the active ingredients are undoubtedly higher than in the blood after intestinal absorption and diffusion in the body. Furthermore, the two flavonoids are able to prevent cell damage due to the virus by enhancing the antioxidant defences through the Nrf2 system and by the direct scavenger action.
\nThe close relationship between cell damage/death and inflammation means that a positive effect can be expected in mitigating the systemic consequences of an inflammation that has eluded controls. Finally, hesperidin and quercetin can exert an indirect beneficial effect, favouring carbohydrate and lipid metabolism, improving general health conditions and thus preventing comorbidities that are contributory causes of the most serious complications. All the experimental models cited here would make it plausible for an increase in the consumption of flavonoid-rich foods, or flavonoid supplementation during periods of increased commitment of the body defences, to help the immune system in the fight against virus infections. It is therefore desirable that further suitable clinical studies are conducted to investigate the potential of these natural substances and to define effective dosages.
\nThe article processing charges were borne by Vanda Omeopatici s.r.l. (Frascati, Roma). The sponsor had no role in the conception, writing or revision of the manuscript.
\nThe author is scientific consultant from Vanda Omeopatici s.r.l. (Frascati, Roma), a company that produces food supplements.
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