horticulturae

Article

The Effect of Organic, Inorganic Fertilizers and TheirCombinations on Fruit Quality Parameters in Strawberry

Neslihan Kilic 1, Aysegul Burgut 2, Muhammet Ali Gündesli 3,* , Gozde Nogay 2, Sezai Ercisli 4,* ,Nesibe Ebru Kafkas 2, Halina Ekiert 5, Hosam O. Elansary 6 and Agnieszka Szopa 5

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Citation: Kilic, N.; Burgut, A.;

Gündesli, M.A.; Nogay, G.; Ercisli, S.;

Kafkas, N.E.; Ekiert, H.; Elansary,

H.O.; Szopa, A. The Effect of Organic,

Inorganic Fertilizers and Their

Combinations on Fruit Quality

Parameters in Strawberry.

Horticulturae 2021, 7, 354. https://

doi.org/10.3390/horticulturae7100354

Academic Editors: Yushan Qiao,

Zhihong Zhang, Jiyu Zhang

and Othmane Merah

Received: 13 August 2021

Accepted: 27 September 2021

Published: 2 October 2021

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4.0/).

1 Department of Organic Farming Management, Kadirli School of Applied Sciences, Osmaniye Korkut AtaUniversity, Osmaniye 80000, Turkey; neslihankilic@osmaniye.edu.tr

2 Department of Horticulture, Faculty of Agriculture, University of Cukurova, Balcalı, Adana 01380, Turkey;yilmaza@cu.edu.tr (A.B.); gozdenogay@gmail.com (G.N.); ebru@cu.edu.tr (N.E.K.)

3 Department of Plant and Animal Production, Nurdagı Vocational School, Gaziantep University,Gaziantep 27310, Turkey

4 Department of Horticulture, Faculty of Agriculture, Ataturk University, Erzurum 25240, Turkey5 Department of Pharmaceutical Botany, Faculty of Pharmacy, Medical College, Jagiellonian University,

Medyczna 9, 30-688 Kraków, Poland; halina.ekiert@uj.edu.pl (H.E.); a.szopa@uj.edu.pl (A.S.)6 Plant Production Department, College of Food and Agricultural Sciences, King Saud University,

Riyadh 11451, Saudi Arabia; helansary@ksu.edu.sa* Correspondence: maligun4646@gmail.com (M.A.G.); sercisli@gmail.com (S.E.); Tel.: +90-442-231-25-99 (S.E.)

Abstract: Strawberry (Fragaria × ananassa Duch.) is widely grown and highly appreciated byconsumers around the world for its delicious, soft, and highly nutritious fruits. Turkey is one ofthe most important strawberry producers in the world. Strawberry cultivation in Turkey typicallyinvolves the use of chemical fertilizers and more recently organic and organic + chemical fertilizershave been started to use in commercial production to produce healthier fruits. Therefore, in thisstudy, we investigated the effect of organic, chemical, and organic + chemical fertilizer treatmentsin strawberry (cvs. ‘Albion’, ‘San Andreas’ and ‘Monterey’) fruit quality parameters includingfruit color (L*, a*, b*, C and h◦) parameters, soluble solids content, total acidity, fruit firmness,vitamin C, specific sugars and organic acids. Results showed that in particular fruit color parameters,soluble solid content (SSC), total acidity, fruit firmness, and vitamin C (L-Ascorbic acid) in fruits ofthree strawberry cultivars were significantly affected by different fertilizer applications (p < 0.05).Compared with conventional chemical fertilizer treatment, the organic fertilizer treatment producedfruit with significantly higher contents of SSC and glucose but decreased fruit firmness and vitaminC. Organic fertilizer also gave more intense colored strawberry fruits with high Chroma values(47,948 in organic fertilizer application and 39,644 and 39,931 in organic + chemical fertilizer andchemical fertilizer, respectively). Citric acid was identified to be the predominant organic acid instrawberry fruits but treatments were found insignificant on citric acid content.

Keywords: strawberry; sugar; vitamin C; organic acids; organic and chemical fertilizer

1. Introduction

Strawberries (Fragaria × ananassa Duch.) are among the widely produced and con-sumed berry fruit in the world. The total cultivation area of strawberries in the world was396,401 ha and total production was 8,885.028 tons in 2019 [1]. The strawberry cultivationarea in Turkey has increased in recent years and it was about 11,679 ha in 2010 to andreached 15,392 ha in 2017. The suitability of ecological conditions in different regions of thecountry promoted the rapid increase of strawberry production [2].

More recently strawberries have gained high praise among consumers for their uniquetaste, availability year-round, and health benefits. In addition, today’s consumers are moreknowledgeable and they are in demand of more attractive, high quality, nutritionallyversatile, and safer plant produce. Strawberry fruits are rich in minerals, vitamins, phenolic

Horticulturae 2021, 7, 354. https://doi.org/10.3390/horticulturae7100354 https://www.mdpi.com/journal/horticulturae

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compounds, and organic acids. The high anthocyanin, total phenolic compounds especiallyellagic acid contents provides anti-carcinogenic and anti-cardiovascular properties [3–5].

As mentioned before strawberry is an important fruit crop in Turkey, but the averageannual productivity in Turkey is considerably lower than in other important strawberry-producing countries like the USA, China, Mexico, Egypt, and Spain [1]. The low productiv-ity for strawberries in Turkey could be the result of soil fertility because most strawberryfarmers in Turkey uses pesticides.

More recently organic strawberry production in Turkey has gained importance becauseit is well known that an organic production system could help reduce the number ofchemicals that damage soils. However, in Turkey, there are very few organic strawberryplantations. It is also important to ensure that there are sufficient nutrients available toensure the good growth of strawberry plantations when using organic fertilizers. Someprevious studies suggest that the productivity of organically produced strawberries islower than conventionally produced ones [6–8]. Therefore, to maximize the potential oforganic strawberry production systems it is important to improve nutrient availability aswell as the abundance and activity of soil microorganisms [9–11].

Previous studies indicated that organically produced fruits and vegetables containhigher levels of flavonoids, anthocyanins, total phenolic compounds, sugars, organic acids,and L-ascorbic acid [12–16]. The increased concern of the consumers about the negativeeffects of agro-chemicals, driven an upward trend in organic production [17,18]. Thistrend also changed the way of scientific studies, where most of them focused on the effectsof organic production on food quality [19–21]. Odongo et al. [22], reported that manure(containing favorable amounts of macro and micronutrients) treatments enhanced fruit setand size in strawberries by the formation of carbohydrates compared to inorganic triplephosphate fertilizer treatment. The use of organic fertilizers plus mineral fertilizers hasproven to be a sound soil fertility management strategy in many countries around theworld. It is not only improving the quality of fruits but also provides sustainability inproduction for the long term [23]. A lot of previous studies have shown that the applicationof organic fertilizers in strawberry fields improves plant nutrient availability and thuspromotes plant growth [24–28]. In addition, the latest studies have focused on the nutrientand phytochemical contents of strawberries and the factors affecting the compositionof this fruit. As a result of these studies, some of the authors reported that especiallyorganically grown strawberries showed similar or better fruit quality characteristics thanconventionally grown strawberries [18,29,30]. Ates et al. [31] reported that the positiveeffects of various natural fertilizers on the yield parameters of strawberry cv. Albionberries (Fragaria × ananassa L.). Reganol et al. [18] implied that the organic strawberryfarms produced higher quality fruit and that their higher quality soils may have greatermicrobial functional capability and resilience to stress. In addition, Cayuela [32] reportedthat organically grown strawberry fruits had higher sugar and dry matter (DM) content,while [33] found similar sugar content between organic and conventionally grown fruits.Despite the higher content of compounds important for human health in organically grownstrawberries, there is still debate about the systematic differences in nutrition and qualityof parameters of organic and traditionally grown strawberry crops [33–35]. Moreover, theexcessive usage of chemical fertilizers and pesticides is very important, particularly fruitswhich can be eaten without removing peels such as strawberries and organic fertilizer mayhave solved this problem through an organic farming system [34–39].

To increase the attractiveness of the fruits by the consumer, the fruit quality character-istics such as firmness, color, and aroma of the fruits are very important. It is now clearthat strawberry production is increasing in Turkey while the studies on the feasibility oforganic fertilizer treatments are insufficient. Thus, the objective of the present study was toevaluate the influence of organic fertilizer, chemical fertilizer, and organic + chemical fertilizertreatments on the color values, fruit firmness, SSC, total acidity, individual sugars, vitamin C,and organic acids of three strawberry cultivars (‘Albion’, ‘San Andreas’ and ‘Monterey’).

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2. Materials and Methods2.1. Plant Material

This study was conducted at the Experimental and Research area of Kadirli VocationalSchool and Instrumental Analysis laboratory of Horticulture Department at the Universityof Çukurova during the 2018–2019 growing periods. Plant materials of the present studyare frigo plants (cold-stored bare root crowns) of ‘Albion’, ‘San Andreas’, and ‘Monterey’cultivars. ‘San Andreas’ strawberry cultivar is a moderate day-neutral with a productionpattern very similar to ‘Albion’ cultivar. Plant vigor for ‘San Andreas’ is somewhat higherthan for ‘Albion’ early in the season, but berry size throughout the fruiting season issimilar to ‘Albion’. The fruit color for ‘San Andreas’ is slightly lighter than ‘Albion’,and it has similar post-harvest characteristics. The flavor of ‘San Andreas’ is very good,suitable for post-harvest handling and it also shows good disease resistance. Comparedto ‘Albion’, the fruit color of ‘San Andreas’ is lighter, very early, and moderate toleranceto several strawberry diseases. ‘Albion’ cultivar is a day-neutral plant characteristic andwell adapted to cool temperate areas. The fruit quality is excellent. It shows a strongtolerance against anthracnose, Verticillium, and Phytophthora, which are well-known asthe most common strawberry diseases. ‘Monterey’ strawberry cultivar is also a day-neutralplant characteristic and slightly stronger flowering than ‘Albion’, with a similar productionpattern. Compared to ‘Albion’, fruits are larger but softer. The fruit has an attractive aroma.It is susceptible to powdery mildew disease. The plant is more vigorous and may requiremore space than ‘Albion’. The fruits are large, firm, slightly carved, and dark red.

2.2. Soil Sampling and Analyses

Soil parameters of experimental area soils (Table 1) were analyzed before the experi-ment according to [40–44].

Table 1. Basic soil data of the experimental site.

Soil Properties Depth (0–20 cm) Depth (20–40 cm)

Texture Clay-loam Clay-loam

pH 7.50 7.50

Saliniy (%) 0.001 0.001

Lime (%) 38.68 36.75

Organic Matter (%) 1.36 1.23

P2O5 (kg/da) 2.17 2.06

K2O (kg/da) 39.33 32.14

Ca (%) 0.09 0.08

Mg (%) 0.04 0.03

Na (%) 0.33 0.29

Fe (mg kg−1) 0.8 0.44

Cu (mg kg−1) 0.62 0.59

Mn (mg kg−1) 1.64 1.91

Zn (mg kg−1) 0.24 0.24

The liquid organic fertilizer (botanica) was used in current research as an organicfertilizer. It is rich in water-soluble plant nutrients, and humic-fulvic acid was also usedin fertilizer applications. Liquid organic fertilizer contains 50% organic matter including21.3% organic carbon, 3% total nitrogen, and 2.5% water-soluble potassium oxide (K2O).Chemical fertilizer application was done according to the soil analysis results.

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The cold stored frigo plants of three strawberry cultivars were provided by YaltirAgriculture company in Adana provinces of Turkey. In the planting stage, N-P-K (15-15-15)fertilizer, chemical fertilizer, and 1/2 organic + chemical fertilizer were sprinkled into thearea before planting and mixed into the soil. Then the planting beds were prepared. Dripirrigation pipes were placed on the stretcher and then covered with black plastic mulch.The frigo plants were planted into 9 × 9 × 9 cm pots in August and rooted under a mistpropagation system and plants were obtained and transplanted on 9 November 2018 to thefield. The seedlings were cultivated on the bed with a 30 cm distance between plants andbetween rows, after planting; 500 g of organic liquid fertilizer was applied to the 1 da ofresidues. Plants were then covered with polyethylene with a low tunnel to protect themagainst the winter cold. Three weeks after the planting phase, weekly organic, chemicaland organic + chemical fertilizer applications were started. In the organic treatments,above the mentioned liquid, organic fertilizer was used in a concentration of 500 g/da on aweekly basis. In the chemical fertilizer experiment, a total of 12.12 kg/da N, 11.35 kg/da P,20.25 kg/da K, and 120 g/da Mg were given as chemical fertilizers during the experiment.The sources of chemical fertilizers are 21% ammonium sulfate, mono ammonium phosphate,potassium sulfate, and magnesium sulfate. In organic + conventional fertilizer application,half of the fertilizer doses of the chemical fertilizer and organic fertilizer treatment are given.Cultural maintenance was carried out regularly during the trial. Fruits were harvested atthe commercial ripening stage (75% red) of strawberry fruits were immediately transferredto the laboratory under cold chain conditions and color measurement and fruit firmnessof strawberries were done immediately after harvest and samples were frozen at −80 ◦Cuntil analysis. For further analysis, fruits were homogenized using a kitchen hand blender.Three replicates were done per analysis total of 30 fruits were used for each replication.The following chemical parameters such as fruit firmness, fruit color, soluble solids content,total acidity (citric acid and malic acids), L-ascorbic acid (vitamin C), sucrose, glucose, andfructose were determined in strawberries using standard methods as below.

2.3. Surface Color Measurement

Color coordinates were measured as L, a*, b* using Minolta chromometer and cal-culated by a formula and given also as C and hue (h◦) values of the outer color of thefruits [45,46].

2.4. Measurement of Fruit Firmness, Soluble Solids, and Total Acidity

At each sampling, 30 fruits per treatment with three replicates were used to measurefruit firmness. Fruit firmness was measured at the equator at two opposite spots (hence,n = 60), using a digital penetrometer (model 53205, TR). The total soluble solids contentwas measured on the juice of 30 fruits, by a digital table refractometer (HI96811; Hannainstruments). The total acidity was measured by titrating the same solution with 0.1 Nsodium hydroxide until reaching pH 8.1 (n = 10), and the results were expressed as %acid [46].

2.5. Sugar Content Measurement

Glucose, fructose, xylose, and sucrose content in the juice obtained from the harvestedstrawberries were determined by [46,47]. Before analysis, frozen juice samples werethawed at 25 ◦C 1 mL of juice was added to 4 mL of ultrapure water (Millipore Corp.,Bedford, MA, USA). The reaction mixture was placed in an ultrasonic bath and sonicatedat 80 ◦C for 15 min and then centrifuged at 5500 rpm for 15 min and it was filteredbefore HPLC analysis (Whatman nylon syringe filters, 0.45 µm, 13 mm, diameter). Thehigh-performance liquid chromatographic apparatus (Shimadzu LC 20A VP, Kyoto, Japan)consisted of an in-line degasser, pump, and controller coupled to a Refractive index detector(Shimadzu RID 20A VP) equipped with an automatic injector (20 µL injection volume)interfaced to a PC running Class VP chromatography manager software (Shimadzu, Japan).Separations were performed on a 300 mm × 7.8 mm i.d., 5 µm, reverse-phase Ultrasphere

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Coregel-87C analytical column (Transgenomic) operating at 70 ◦C with a flow rate of0.6 mL min−1. Elution was isocratic ultrapure water. Individual sugars were calculatedbased on their standards and expressed in % of FW.

2.6. Organic Acid Measurement

Organic acids in strawberry fruit juice were determined by HPLC analysis developedby Bozan [48]. For organic acids extraction, 1 mL of the sample, and 4 mL of 3% metaphos-phoric acid were mixed. The mixture was placed in the ultrasonic water bath at 80 ◦C for15 min and it was sonicated and centrifuged at 5500 rpm for 15 min. Afterward, the mixturewas filtered (Whatman nylon syringe filters, 0.45 µm, 13 mm, diameter) and the HPLC vialswere removed. The extract of organic acids was analyzed using a high-performance liquid chro-matographic apparatus HPLC (Shimadzu LC 20A VP, Kyoto, Japan) equipped with a UV detector(Shimadzu SPD 20A VP) and we used an 87 H column (5 µm, 300 × 7.8 mm, Transgenomic).As for the operating conditions column temperature, was set at 40 ◦C; injection volume,20 µL; detection wavelength, 210 nm; flow rate 0.8 mL/min. and % 0.05 mM sulphuric acidwas used as the solvent. Identification of organic acids and determination of peaks is basedon the retention times of peaks and comparison of spectral data according to standards.The identified acids were evaluated according to the relevant standard calibration curves.

2.7. Statistical Analysis

All the result data were processed with the SPSS package program version 16.0 (SPSSInc., Chicago, IL, USA). All data were presented as the mean ± standard error (SE) andanalyzed by one-way analysis of variance (ANOVA). Differences were considered signifi-cant at p < 0.05. Additionally, principal component analyses (PCA) were also performed toshow the relationships between the parameters and the cultivars. As an output of the PCA,in a biplot, the length of the lines approximates the variances of the variables. The longerthe line, the higher is the variance. The cosine of the angle between the lines approximatesthe correlation between the variables they represent. The closer the angle is to 90, or270 degrees, the smaller the correlation. An angle of 0 or 180 degrees reflects a correlationof 1 or −1, respectively. Cut-points far off in the direction of the variable line indicate highvalues, while cut-points far off on the variable line, which has been extended through theorigin, represent low values. Finally, the distance between two points approximates theEuclidean distance between two observations in the multivariate space. Observations thatare far away from each other have a high Euclidean distance, and vice versa [49].

3. Results and Discussion3.1. Surface Color Measurement

Color is one of the most significant quality parameters for evaluating strawberries.The color in strawberries has been attributed to many factors, including maturity, ecology,genotype, and cultivar [26,32].

Results showed that there is a significant difference among the treatments (Table 2).The brightness (L) color was noted from the ‘San Andreas’ cultivar (35.619) which hadbeen fertilized with the chemical fertilizer. On the other hand, the lowest external lightnesswas found in the ‘Albion’ fruits (19.403) with organic fertilizer treatment. As the averageof three cultivars, the organic fertilizer treatment was then noted to have the lowest Lvalue (24.764) where the highest L value (33.407) was obtained from the chemical fertilizertreatment (Table 2). In a previous study by Crecente-Campo [13], similar results werenoted where they compared the external color brightness value of the strawberry fruits andreported low L values for organic (27.30) and high L values for conventional strawberrycultivations (32.60). When the L value increases as the color is lighten [50]. Pilanalı andKaplan [51] in their experiments, reported that solid humic acid treatments significantlyaffect the fruit color. They noted that solid humic acid treatments increased the organicmatter content of the soil, and this also cause an increase in the L value. However, in thisstudy, the highest lightness values were obtained while chemical fertilizer treatment.

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Table 2. Color values of strawberry fruits as affected by different fertilizer treatments.

Cultivars, Treatments, and Combination L* a* b* C* h◦

Organic * ‘Albion’ 19.403 c 46.831 a 33.744 a 57.835 a 35.521 abOrganic + Chemical * ‘Albion’ 32.763 a 35.612 b 19.589 bc 40.729 bc 28.543 cdChemical * ‘Albion’ 33.435 a 35.321 b 20.673 bc 41.014 bc 30.227 bcOrganic * ‘San Andreas’ 24.186 bc 46.307 a 29.265 ab 52.106 ab 36.815 aOrganic + Chemical * ‘San Andreas’ 33.398 a 34.808 b 20.169 bc 39.933 bc 29.100 cdChemical * ‘San Andreas’ 35.619 a 36.230 b 24.227 abc 42.269 bc 30.306 bcOrganic * ‘Monterey’ 30.704 ab 30.652 b 14.398 c 33.902 c 25.056 cdOrganic + Chemical * ‘Monterey’ 31.249 ab 34.710 b 15.974 c 38.270 bc 24.377 dChemical * ‘Monterey’ 31.167 ab 32.621 b 16.213 c 36.511 c 26.131 cd

‘Albion’ 28.534 a 39.254 a 24.669 a 46.526 a 31.430 a‘San Andreas’ 31.068 a 39.115 a 24.554 a 44.769ab 32.074 a‘Monterey’ 31.040 a 32.661 b 15.528 b 36.228 b 25.188 b

Organic 24.764 b 41.263 a 25.802 a 47.948 a 32.464 aOrganic + Chemical 32.470 a 35.043 b 18.577 b 39.644 b 27.340 bChemical 33.407 a 34.724 b 20.371 b 39.931 b 28.888 b

L*: brightness; a*: red–green axis; b*: yellow–blue axis; C*: color intensity; h◦: tone. * Kruskal Wallis p value, Different capital lettersindicate statistically significant difference among varieties and application at p < 0.05.

Fruit outer color a* value indicates the intensity of the color. The lower the a* value, thelower the red intensity; and the increase in a* value increases the red color intensity [50,51].The highest external color a* value (green-red) of the fruits had been noted from the ‘Albion’cultivars (46.83) treated with organic fertilizer. Thus, the lowest value (32.62) was obtainedfrom the fruits of the ‘Monterey’ cultivar with chemical fertilizer treatment. Overall, the‘Monterey’ cultivar was noted to have the lowest a* value (32.66); where the organic treatedplants had the highest a* values (41.26). In a similar study Ates [31] noted that ‘Monterey’ hadthe lowest a* value as compared with ‘Albion’, ‘Aromas’, ‘Camarosa’ and ‘Sweet Charlie’.

The data obtained for the CIE L* a* b* color (Table 2) was similar to those recorded byWang and Camp [25]. In addition, present results are similar to those of Ayala-Zavala [52]for the surface color for strawberries: L 33.90, C 35.10, and Hue 28.50. Similar to a* values,the highest b* values were noted from the organic fertilizer treatment. Gulbag and Ilgin [53]similarly investigated the effects of potassium humate, vegetable origin liquid humic acid,and seaweed as organic fertilizer in ‘Camarosa’ and ‘Elsanta’ strawberry cultivars. In thatstudy, researchers found that the highest b* value was obtained from the ‘Elsanta’ cultivartreated with seaweed (26.65), and the lowest b* value was obtained from the ‘Camarosa’cultivar treated with potassium humate (22.75).

The highest C value (58.66) was then noted from the ‘San Andreas’ cultivar fertilizedwith organic fertilizer. The lowest color density value (36.45) of the outer fruit was obtainedfrom the ‘Monterey’ strawberry cultivar with chemical fertilizer treatment (Table 2). In astudy, yield and some quality parameters of ‘Monterey’, ‘Albion’, ‘Aromas’, ‘Camarosa’and ‘Sweet Charlie’ cultivars fertilized with different organic fertilizers were examined.The lowest average C values were determined from the ‘Monterey’ cultivar and the highestfrom the ‘Aromas’ cultivar [52]. Moreover, in our experiment the highest value of Hue(color angle value) was noted from the organic treated fruits, while the comparison of thecultivars for Hue resulted in decreasing order of ‘San Andreas’ > ‘Albion’ > ‘Monterey’.

3.2. Measurement of Soluble Solids, Total Acidity, and Firmness

The soluble solid content (SSC), total acidity, and fruit firmness values of threestrawberry cultivars fertilized with different fertilizers are shown in Table 3. We foundstatistically significant differences (p < 0.05) among treatments. The lowest SSC was de-termined as 8.87% (Organic + Chemical-‘San Andreas’ cultivar) and the highest as 10.73%(Organic + Chemical-‘Monterey’ cultivar) (Table 3). Reganold et al. [18] reported that thedry matter content of organically grown strawberries is higher (8.3%) than conventionallycultivated crops. Similarly, Mahedeen [54], determined that organic farming improves

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fruits’ soluble solids contents of strawberries. Ozguven and Yilmaz [55] reported that theamount of SSC in the ‘Fern’ strawberry cultivar varied from 6.30% to 8.44% in their exper-iments on different conditions in Adana. In another study, Ozkan [37] reported that theSSC amount varied between 8.42% and 8.66% on the ‘Fern’ strawberry cultivar in differentorganic fertilizer treatments. Our results differed from previous studies. This situation isthought to be caused by the cultivar, soil, and climate differences of experimental areas.

Table 3. Effect of different fertilizer treatments on SSC, total acidity, and fruit firmness of strawberry cultivars.

Treatments Cultivars SSC(%)

Total Acidity(%)

FruitFirmness (N)

Organic

‘Albion’ 10.53 a 1.45 a 0.95 a

‘San Andreas’ 9.57 b 1.32 b 0.86 b

‘Monterey’ 10.50 a 1.14 c 0.93 a

Organic + Chemical

‘Albion’ 9.17 b 1.30 b 1.16 b

‘San Andreas’ 8.87 c 1.37 a 1.20 a

‘Monterey’ 10.73 a 1.17 c 1.12 c

Chemical

‘Albion’ 9.67 c 1.63 a 1.55 a

‘San Andreas’ 10.60 a 1.46 b 1.25 b

‘Monterey’ 9.97 b 1.35 c 0.92 c

Organic 10.20 a 1.31 b 0.91 c

Organic + Chemical 9.59 b 1.24 c 1.16 b

Chemical 10.08 a 1.48 a 1.24 a

Values are the average of triplicates ± standard deviation. Different letters in each row show the significant statistical difference (p < 0.05)between the samples.

The highest total acidity of the fruits was obtained from the ‘Albion’ cultivar from thechemical fertilizer treatment (1.63%) and the lowest from the organic fertilizer treatment of the‘Monterey’ cultivar (1.14%) and we found statistically significant differences (p < 0.05) amongtreatments (Table 3). Abu-Zahra [56] reported similar findings for the ‘Honor’ strawberrycultivar where the amount of total acidity was higher in conventionally grown fruits. Accordingto Camargo [57] organic and conventionally cultivated ‘Camarosa’ and ‘Sweet Charlie’ cultivarshave significant differences in terms of the amount of total acidity, where the conventionalgrowing system have higher values for ‘Sweet Charlie’ cultivar, but organic growing systemshave higher values for ‘Camarosa’ strawberry cultivar. These results are similar to the findingsobtained in our study.

The effects of organic and chemical fertilizers on fruit firmness were also examined inthe present study (Table 3). According to the results obtained, chemical fertilizer treatmentwas found to have the highest fruit firmness (1.16 N) than the other fruits. It was thenfound that fruits treated with organic fertilizer were softer (0.91 N) than other treatments.‘Albion’ had the hardest flesh fruit under the application of three types of organic fertilizersand ‘San Andreas’ was found to be the softest cultivar.

3.3. Organic Acids

The organic acid content of the fruits varies according to the species, cultivars, andcultivated conditions, etc. Especially sugar-acid balance and contents are the primarydeterminants of the taste properties of fruits. The most widespread acids evaluated infruits are tartaric acid, malic acid, and citric acid, known to affect taste-aroma formationand many physiological processes are known as “fruit acids” [58,59].

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The changes in the organic acids that are quantitatively the most important differencein determining fruit acidity are shown in Table 4. The organic acids (L-ascorbic acid, citricacid, malic acid, succinic acid, and fumaric acid) were identified and quantified by theHPLC method. Statistically significant differences (p < 0.05) occurred among strawberryfruits in terms of the content of organic acids. The highest amount (43.193 mg/100 g) ofL-ascorbic acid was noted from the ‘Albion’ cultivar fertilized with chemical fertilizer while‘San Andreas’ had the lowest (21.678 mg/100 g) L-ascorbic acid content with organic treatment.Likewise, Odriozola-Serrano [60] found that the vitamin C value of strawberry cultivar was49.5 mg/100 g. These values are within the range observed in other studies. Klopotek [61]reported that vitamin C contents were ranged between 37 and 69 mg/100 g in diversestrawberry juices. The U.S recommended daily intake (RDI) of vitamin C is currently revisedrecommended to should not be below 60 mg [52]. Reganold [18] report that organically grownstrawberries have higher levels of vitamin C than conventionally grown strawberries. Abu-Zahra [47] similarly noted that the organic fertilized strawberry fruits have higher vitamin Cthan the control and conventionally grown fruits. Cayuela [30] did not show the relationshipbetween a higher level of vitamin C and organic cultivation. In the study of Hagg [62],the strawberry samples of the cultivar ‘Senga Sengana’ contained 52–64 mg vitamin C per100 g. The findings of our study conducted on vitamin C in strawberries are also generallyin agreement with the findings of the other researchers [62,63]. Ozkan [37] reported thatthe organic treatment of the ‘San Andreas’ cultivar has the lowest value of vitamin C thanthe others.

Table 4. The organic acid content of strawberry fruits is affected by different fertilizer treatments.

Cultivars, Treatments, orCombination

L-Ascorbic Acid(mg/100 g) Citric Acid (%) Malic Acid

(%)Succinic Acid

(%)Fumaric Acid

(%)

Organic * ‘Albion’ 29.835 bc 0.920 abc 0.315 ab 0.278 a 0.009 NS

Organic + Chemical * ‘Albion’ 28.703 bc 0.852 abc 0.269 ab 0.225 a 0.009Chemical * ‘Albion’ 43.193 a 1.184 a 0.384 a 0.265 a 0.010Organic * ‘San Andreas’ 21.678 c 0.816 bc 0.244 b 0.218 a 0.007Organic + Chemical * ‘San Andreas’ 24.362 bc 0.893 abc 0.267 ab 0.255 a 0.008 NS

Chemical * ‘San Andreas’ 34.533 ab 1.137 ab 0.371 ab 0.287 a 0.001Organic * ‘Monterey’ 26.748 bc 0.678 c 0.312 ab 0.299 a 0.009Organic + Chemical * ‘Monterey’ 29.803 bc 0.723 c 0.320 ab 0.290 a 0.010Chemical * ‘Monterey’ 31.607 bc 0.655 c 0.328 ab 0.266 a 0.015

‘Albion’ 33.911 a 0.986 a 0.322 a 0.254 a 0.009 NS

‘San Andreas’ 26.858 a 0.948 a 0.294 a 0.255 a 0.080‘Monterey’ 29.386 a 0.689 b 0.319 a 0.285 a 0.010

Organic 26.087 b 0.809 NS 0.288 b 0.262 NS 0.009 NS

Organic + Chemical 27.623 b 0.823 0.285 b 0.257 0.009Chemical 36.444 a 0.993 0.361 a 0.272 0.015

Values are the average of triplicates ± standard deviation. * Kruskal Wallis p value, Different capital letters indicate statistically significantdifference among cultivars at p < 0.05. NS: Non-Significant.

The most common acids found in fruits are tartaric, malic, and citric acid. In thepresent experiment, the highest citric acid amount (1.184%) was observed in the ‘Albion’cultivar with chemical fertilizer treatment while ‘Monterey’ had the lowest (0.655%) citricacid content with chemical fertilizer treatment. The highest amount of malic acid content(0.769%) of ‘Albion’ fruits were detected under chemical fertilizer treatment. ‘San Andreas’cultivated with organic fertilizer was found to have the lowest amount malic acid content(0.244%) among the strawberry cultivars. The highest amount of succinic acid content(0.299%) of ‘Monterey’ fruits was detected under organic fertilizer treatment (Table 3). Inthis study, the highest total acid content in the ‘Albion’ cultivar was obtained from chemicalfertilizer treatment while the lowest acid content was obtained from organic fertilizedfruits of the ‘San Andreas’ cultivar (Table 3). Holcroft and Kader [64] and Mahmood [65],reported that citric acid is the most abundant organic acid in strawberry fruits, followed

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by malic acid. In addition, Kafkas [46] reported that the main organic acid is citric acidand its concentration varied between 9.15 and 20.27 g/kg frozen weight based on thematuration stages in strawberries. Kafkas [66] found the amount of citric acid was 0.61%in the ‘Camorosa’ strawberry cultivar and 0.91% in the ‘Dorit’ cultivar. Koyuncu andDilmaçünal [59], reported that the amount of citric acid in the strawberry fruits decreasedduring storage and it was found to as 5.27 mg/g at the end of the storage. Kafkas [66]examined the organic acid content in three different maturity periods in strawberries andthey found that malic acid content varies between 0.10% and 0.43% in the green period.Some research found that the content of total acids in strawberries amounted to 1.00%,while other research found that this value was within the range from 0.98–1.20% [67–71].While some of the data obtained from this study were close to the values reported in otherstudies, it was observed that they were higher than the values in some studies and lowerthan others. These differences can be attributed to different genetic characteristics of thestudy materials, as well as climatic conditions and other environmental factors.

3.4. Sugar Contents

Together with acids, sugars are the main ingredient in the fruit’s flavor. The content oftotal sugar varies depending on the variety, degree of maturity, and growing conditions. Themost common sugars in strawberry fruits are sucrose, glucose, and fructose [62,63]. There werestatistically significant differences between treatment and cultivars in terms of sugar contents(p < 0.05) (Table 5). In this research, the amount of fructose and glucose was determined at thehighest level (4.044%) and (3.535%) in fruits of organic + chemical treated ‘Albion’ cultivar,respectively (Table 5). Urun et al. [72], Montero [73], and Perkins-Veazie [74] also found higherconcentrations of fructose than other sugars in ripe strawberry fruits. On the other hand, boththe results of the present study and other published literature had found quantitative smalldifferences between glucose and fructose. While the highest amount of glucose (3.535%) wasfound in the organic + chemical treated ‘Albion’ strawberry fruits, the lowest glucose content(2.713%) was noted from the organic + chemical treated ‘San Andreas’ strawberry fruits. Inthis study, the sucrose content of organically fertilized ‘San Andreas’ strawberry fruits wasfound to be 1.032%, while the organic fertilized ‘Monterey’ cultivar was found to be 1.741%.Cayuela [30] found that organic berries have a higher sugar content than conventionallygrown fruits. Pérez [75] reported 5.15, 17.77, and 19.40 g/kg values for sucrose, glucose, andfructose, respectively, for the ‘Chandler’ strawberry cultivar. Al-Karawi and Al-Rawi [76]found that organic fertilizer treatments increased sugar content in strawberry fruits. Similarly,Neri [77] reported that long-term organic fertilizer treatments increased the sugar contentof fruits of the ‘Onda’ strawberry cultivar. Mahmood [65] reported that amounts of sucrose,glucose, and fructose are in the immature to fully mature stages in strawberry cultivars were1.79–2.86%, 1.79–2.25%, and 0.01–0.25%, respectively. The findings of the present study aregenerally in agreement with the findings of the other researchers [71,72,75,78].

Table 5. The sugar content of strawberry fruits is affected by different fertilizer treatments.

Cultivars, Treatments, or Combination Sucrose (%) Glucose (%) Fructose (%)

Organic * ‘Albion’ 1.283 NS 3.263 NS 3.757 NS

Organic + Chemical * ‘Albion’ 1.402 3.535 4.044Chemical * ‘Albion’ 1.328 3.123 3.573Organic * ‘San Andreas’ 1.032 2.820 3.239Organic + Chemical * ‘San Andreas’ 1.308 NS 2.713 NS 3.165 NS

Chemical * ‘San Andreas’ 1.308 3.006 3.494Organic * ‘Monterey’ 1.741 3.272 3.724Organic + Chemical * ‘Monterey’ 1.646 3.041 3.455Chemical * ‘Monterey’ 1.432 2.766 3.170

‘Albion’ 1.338 ab 3.307 a 3.791 a‘San Andreas’ 1.216 b 2.846 b 3.299 b‘Monterey’ 1.606 a 3.027 ab 3.450 ab

Organic 1.352 NS 3.118 NS 3.573 NS

Organic + Chemical 1.452 3.096 3.555Chemical 1.356 2.965 3.412

* Kruskal Wallis p value, Different capital letters indicate statistically significant difference among cultivars at p < 0.05. NS: Non-Significant.

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3.5. Statistical Analyses Results

Correlation analysis was also conducted to statistically reveal the effect of organicand chemical fertilizer treatments on organic acid, fruit firmness, and sugar content ofstrawberry fruits (Figure 1). Results showed that the organic acid contents have negligibleto moderate negative correlation with the a*, b*, C, and Hue values of color. The highestnegative correlation for color values was noted to be with the sucrose content. So, it can beconcluded that the increase in sucrose content reduces the a*, b*, C, and Hue values, or viceversa. On the other hand, L-ascorbic acid was found to have a strong positive correlationwith the malic and fumaric acid contents. Stojanov [79] reported MCB (aged mature cattlemanure as organic fertilizer) and Scotts (water-soluble granulated compound fertilizer,commercially named) significantly improved single and total sugars contents. Ozkan, [37]reported the effect of organic fertilizers and chemical fertilizer treatment on the strawberrycultivar ‘Fern’. Sugar content is an important criterion of taste in strawberry fruits andattracts consumers [66,80].

Figure 1. Correlation graphic for organic acids, sugars, and color parameters of strawberry fruits asaffected by different organic or chemical fertilizer applications.

Principal component analysis (PCA) was conducted to determine the relationshipsamong the quality parameters and cultivars (Figure 2). As a result of this statistical analysis,the most important parameters that define the ‘Albion’ cultivar were found to be theL-ascorbic acid, fructose, and glucose. On the other hand, the ‘Monterey’ cultivar was foundto be highly affected based on sucrose and succinic acid content, while the ‘San Andreas’cultivar was found to having no strong relationships with any of the tested parameters.Maybe the most important results of the present study are presented in Figure 2 where thecolor values have a strong relationship with the organic fertilizer treatments. These resultssupport our above-discussed effects of organic fertilization on the color values. It waspresented in the figure that the organic acids are highly improved by the chemical fertilizertreatment. Finally, the combination of organic and chemical fertilizers has been found toprovide the highest sucrose content to the strawberries.

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Figure 2. PCA-Biplot graph for organic acids, sugars, and color parameters of strawberry fruitsas affected by different organic or chemical fertilizer treatments, grouping for cultivars (up), andgrouping for fertilizers (down).

4. Conclusions

There are a limited number of studies in the literature on the biochemical contents ofstrawberry fruits in organic fertilizer conditions. Specifically, the study involved a range ofcomparative fertilizer treatments and therefore this study is considered a valuable referenceto determine the most suitable treatments and cultivars for commercial production. Thefindings of the present study also suggested that the organic fertilizer significantly improvesthe color of the strawberry fruits and it is also required to apply chemical fertilizerstogether to obtain high-quality strawberries. In conclusion, we need standardized testing,extraction, and analysis protocols to compare cultivars grown in different countries. Thisresearch will certainly be helpful in better understanding the organic farming packagefor strawberries as a holistic and sustainable approach to improve soil health as well asincrease the productivity and profitability of quality fruits.

Author Contributions: Conceptualization, N.K.; N.E.K.; G.N.; A.B. and M.A.G.; writing—originaldraft preparation, N.E.K., N.K.; S.E.; A.B., G.N. and M.A.G.; writing—review and editing, N.K.,A.B., M.A.G., H.E.; A.S.; S.E.; H.O.E. and N.E.K.; methodology, N.K., N.E.K., G.N., M.A.G., and A.B.;executed the experiment, M.A.G., N.K.; N.E.K.; G.N.; A.B. and S.E.; formal analysis, M.A.G., N.E.K.;A.B.; N.K. and G.N. All authors have read and agreed to the published version of the manuscript.

Funding: This research received external funding from Researchers Supporting Project number(RSP-2021/118), King Saud University.

Institutional Review Board Statement: Not applicable.

Informed Consent Statement: Not applicable.

Data Availability Statement: All-new research data were presented in this contribution.

Acknowledgments: The authors extend their appreciation to King Saud University (RSP-2021/118),Riyadh, Saudi Arabia, for their support of the present research manuscript.

Conflicts of Interest: The authors declare that they have no conflict of interest.

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