Available online freely at www.isisn.org Bioscience Research Print ISSN: 1811-9506 Online ISSN: 2218-3973 Journal by Innovative Scientific Information & Services Network REVIEW ARTICLE BIOSCIENCE RESEARCH, 2021 18(1): 889-898. OPEN ACCESS

The importance of ( limon) and the future of its cultivation by using bio-fertilizers

Salem Abdelmoaty1, Mohammad Moneruzzaman Khandaker*1, Noor Afiza Badaluddin1, Khamsah Suryati Mohd1, Umar Aliu Abdullah1, Nurul Elyni Mat Shaari1, and Khairil Mahmud2

1School of Agriculture Science & Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, Besut Campus, 22200 Besut, Terengganu, Malaysia 2Department of Crop Science, Faculty of Agriculture, Universiti Putra Malaysia, Seri Kembangan 43400, Selangor, Malaysia

*Correspondence: [email protected] Received 10-12-2020, Revised: 09-03-2021, Accepted: 10-03-2021 e- Published: 15-03-2021 Lemon trees (Citrus lemon L.) are among the trees scattered in Southeast Asia, especially Malaysia, The importance of has increased in recent times, especially after the spread of the Covid-19 epidemic around the world, as lemon juice rich in vitamin C is fortified for the immunity of the human body. Also, it is an important source of Flavonoids, known as antioxidants, which remove free radicals that damage tissue cells within the body. Bio-fertilizers are products containing multiple genera of microorganisms in large numbers and beneficial to both and soil in an integrated manner. In addition bio-fertilizers have proved that increase the nutrient content inside plants, whether in leaves or ,which is reflected in the quantity and quality of fruits and also balance the ratio between nutrients in the soil. This review discussed the nutritional and health benefits of lemon and the importance of bio-fertilizer on growth, yield and fruit quality of lemon. Keywords: Citrus, human benefits, cultivation, bio-fertilizer

INTRODUCTION Table 1: World Lemon production in 2018 Family includes many genus, but (Adapted from (FAOSTAT). 2019. the most important of them is the citrus genus, Retrieved February 2020 which is famous for its numerous nutritional and Lemon (and ) therapeutic properties in addition to the cosmetic production, 2018 (in millions of tons) properties of its flowers and fruits, one of the best Country 2018 known and most used species of the genus Citrus

India 3.1 is the lemon. Some genomic studies of the lemon Mexico 2.5

indicated that it was a between bitter China 2.5

(sour orange) and (Gulsen and Argentina 2.0

Roose, 2001; Zhiqin, 2011).There are studies Brazil 1.5 indicated that Citrus limon is probably hybrid Turkey 1.1 between Citrus aurantium and Citrus medica that World 19.4 The lemon, Citrus limon (L.) is small trees through analyzed the origin ofseveral species of belongs family Rutaceae whose evergreen trees, genus citrus including Citrus limon (Talon and it is believed that the origin of the lemon is South Gimmter, 2008) and (Jing et al. 2015). Asia, primarily North eastern India, northern Salem et al. Imortance of lemon and its cultivation by using bio-fertilizers

Burma or China Morton (1987). World production bud induction start-up begins after exposure to of lemons (combined with limes for reporting) was low hot temperatures, after which the full flowering in 2018 as 19.4 million tons according to stage, and the flowers appear either individually or FAOSTAT, (2019) (Table 1). in groups on the axes of the leaves. The pollen The top producers – India, Mexico, China, grains are sticky and the flowers either cross or Argentina, Brazil, and Turkey – collectively self-pollinate by insects that are attracted to the accounted for 65% of global production. strong scent of the flowers, next stage is fruit set and the last stage is fruit ripening (Figure 2). The Botanical Characteristics fruits go through three main growth stages, the Citrus limon (L.) Burm is a tree with evergreen first stage takes about two months (the slow leaves and yellow edible fruits from the growth stage), where it begins with the rapid family Rutaceae, the tree reaching 2.5–3 m in division of cells and then the second stage (the height. It has evergreen leaves leathery ovoid in rapid growth stage) where the size of the cells shape, the margin serrate with sharp spines in the increases significantly in size by enlarging the size axils of the stalks. Flowers are gathered in small of the cells and the accumulation of water and the clusters or occur individually, growing in leaf axils, juice within the fruit and this stage takes about it is bisexual flowers are white with a purple tinge four months and finally the third stage, which is at the edges of the petals each flower has five the period of ripening of the fruit, where it often petals (Figure 1). The fruit is berry as an oval stops growing and undergo a non-climacteric shape, its colour turns from green into yellow process ( Domingo et al. 2007). during ripening, with apical nipple, the pulp forms 8-10 segments contains acidic juice. The fruit Variety of lemon consists of three parts, the first is the exocarp or Lemon varieties fall under two types: true it is full of with oil glands, which is a thick lemon it has few varieties, and hybrid lemon it has outer shell that turns yellow at maturity and in many varieties, in general many lemon varieties some varieties it remains green, the middle part is differ among them in terms of the colour of the the mesocarp or albedo is a white spongy part fruit, pulp colour, the degree of acidity fruit teats that is rich in pectin materials and the inner part is and the number of seeds. These some varieties endocarp which contains the juice contain organic include the following: acids and sugars with water, it is definitely acidic in taste. The seeds are small oval white or Eureka: yellowish-white in colour some fruits are seedless. It is a well-known popular kind of lemon. It is (Mabberley, 2004). considered a true lemon (without hybrid). Its trees are sensitive to cold and the tree reaches a height Flowering and fruit development of lemon of 20 feet that gives a crop throughout the year, Lemon trees bloom almost all year round, and the fruits are yellow in colour and the pulp is the main flowering occurs in the spring, the flower greenish yellow (Figure 3).

Figure 1: The floral structure and fruits of lemon (Adapted from Köhler, 1898).

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Salem et al. Importance of Lemon and future of its cultivation by using bio-fertilizers

Figure 2: Stages of fruit set and fruit ripening of citrus (Adapted from Domingo et al., 2007).

Figure 3: Eureka and Myer lemon (Adapted from University of Florida, IFAS Gardening Solutions Citrus) Myer: hybrid variety (lemon & orange mandarin), a wide variety, it is believed to be its Lisbon: origin is China. The trees are cold-resistant, the True lemon, its production is a little compared colour of the fruit is light orange, and the pulp is to the variety Eureka, cold resistant, the fruits are pale orange-yellow, moderately acid taste with yellow in colour and rough texture, the pulp pale few small seeds (Morton, 1987). greenish yellow that contains a small number of : (Citrus aurantifolia) or (limau nipis seeds and very acidic taste. as known in Malaysia), popular in Malaysia, Fruits

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Salem et al. Importance of Lemon and future of its cultivation by using bio-fertilizers are green, pale, yellowed, and round, the peel of Table 2: Proximate analysis of lemon (100 g of the fruit contains antibacterial substances and is lemon) used in medicines (Noman, 2015). Name Amount Unit Lime: (Citrus microcarpa) or Water 88.98 g (limau kasturi as known in Malaysia) Widespread Energy 29 kcal in Malaysia, believed to be from China. Fruiting Protein 1.1 g almost all year, but the climax is between August Total lipid (fat) 0.3 g and October, the tree is a small with long roots, Carbohydrate, by difference 9.32 g and fruits are greenish-yellow in color and ripen Fiber, total dietary 2.8 g after five months of flowering. Abdullah et al., Sugars, total including NLEA 2.5 g (2012). Calcium, Ca 26 mg Iron, Fe 0.6 mg Nutrition and phytochemicals: Magnesium, Mg 8 mg Phosphorus, P 16 mg Nutritional benefits Potassium, K 138 mg Lemon is widely used, the fruits can be used Sodium, Na 2 mg fresh to make a juice called , which is a Zinc, Zn 0.06 mg Copper, Cu 0.037 mg refreshing drink that contains a high percentage of Selenium, Se 0.4 µg vitamin C (Table 2). Also, the fruit content can be Vitamin C, total ascorbic acid 53 mg used as a natural flavour and preservative added Thiamin 0.04 mg to different foods and can be added to other foods Riboflavin 0.02 mg such as salad dressing, sauces and baked goods. Niacin 0.1 mg It is also used in the manufacture of soft drinks Vitamin B-6 0.08 mg and the addition of the acidic taste of food Folate, total 11 µg products (González et al., 2009). It is also can be Folate, food 11 µg added to fish and meat for marinades them, as it Folate, DFE 11 µg works to convert amines in fish into non-volatile Choline, total 5.1 mg ammonium salts, as partially hyardlyzes Vitamin A, RAE 1 µg tough collagens the hard fibers in the meat and Carotene, beta 3 µg tenderizing them to become easy for cooking. Carotene, alpha 1 µg Lemon juice is frequently added to pancakes in Cryptoxanthin, beta 20 µg some countries, the juice is commonly added to Lutein + zeaxanthin 11 µg tea to add a refreshing flavor (Siti et al. 2017). Vitamin E (alpha-tocopherol) 0.15 µg Some fruits after being sliced them tend to Fatty acids, total saturated 0.039 µg oxidation after they are exposed to air and turn to brown colour (enzymatic browning), such as Cosmetic uses of lemon bananas, apples and avocados, lemon juice Lemon oil has been used since the 18th added to them to prevent this oxidation in the century in the production of the famous ‘Eau de short term. Also, some cheeses curdled only by Cologne’ and the essential oils. Currently, lemon acidity, so lemon juice is using to curdle the milk is increasing in use for cosmetic purposes due to for cheese productions. (Science Learning Hub its multiple benefits. In Tanzania, lemon juice is 2012). Methanol extract from the peel of Citrus mixed with honey, cucumber and egg albumin and microcarpa, Citrus reticulata and Citrus sinensis applied to the skin every night, these ingredients has antibacterial activity, especially smooth the skin face and help treat acne. Staphylococcus aureus and E. coli (Maahendran (Maregesi et al.2014). A group of 36 plant et al. 2013). Lemon juice 1% used with other species, including Citrus limon, were used as some aqueous colloid to improve the physical and cosmetics in Cameroon, and a group of 78 chemical properties of the semi-dried, convulsive cosmetic recipes were prepared using these catfish and extend its shelf life (Ishamri et al. plants, such as face masks, body cream and hair 2017; Nua and Noor, 2020). cream (Fongnzossie et al. 2017). In Palestine,

fresh lemon juice is mixed with olive oil and then

applied to the scalp, this mixture is used to treat

hair problems and disorders. (Ziad et al. 2017).

Studies have proven the effect of citric acid as an

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Salem et al. Importance of Lemon and future of its cultivation by using bio-fertilizers antioxidant, and therefore it is used recently in the of vitamin C, as well as treatment of obesity and technology of anti-aging cosmetics where vitamin prevention of AIDS by strengthening the human C works to combat oxidative stress in the skin immune system (Mabberley, 2004). It has also cells and increases the production of collagen proven effective in treating respiratory diseases responsible for protecting the skin, so it is use for like coughs (Papp et al. 2011). reducing shallow wrinkles in anti-aging products. Several clinical studies have shown that (Manconi et al. 2016). lemon juice is useful in preventing kidney stones formation and reducing the accumulation of Medical benefits of lemon calcium oxalate by increasing the levels of citrate When massaging muscles with materials that in the urine and thus preventing the recurrence of contain lemon peel oil, this relaxes them and is stone formation. (Clement et al. 2015). In study used in cases of muscle spasm, as it helps to using some plants for treat ethnogynecological, calm the nerves and deep relaxation. (Millet, this study revealed that lemon is of great 2014) but, lemon oil should not be used in high importance in treating menstrual disorders in concentrations in cosmetics or directly on the skin women and its use has been documented because D lemonene - a component of lemon oil - successfully in this regard. (Bhatia et al. 2015). has an allergic effect, and direct exposure to Vitamin C helps ward off infection, and is used to sunlight after use is prohibited. (Tammaro et al. treat scurvy, sore throat, fever, rheumatism, HBP, 2017). Kanmani et al. (2014) and Dimopoulou et and chest pain. Aquatic chemicals from lemons al. ( 2019) reported that, the peel used in the have been discovered such as phenolic acids, manufacture of pectin, which is used as a gelling flavonoids, triterpenoids, carotenoids, essential agent, including the production of jams and jellies oils, and tannins, while it has a series of in food industrial, and as thickener, texturizer, pharmacological benefits such as anticancer, emulsifier and stabilizer in dairy products, also it hypoglycemia, anti-obesity, antimicrobial, antiviral, can be used in pharmaceutical, dental and and antiviral for hyperlipidemia, cosmetic formulations. Lemon extract can be used hypercholesterolemia, antihypertensive, anti- to develop safe antibacterial and antifungal inflammatory, analgesic and tonic for the liver compounds or a treatment for upper respiratory have been reported. (Balogun and Ashafa, 2019). infections (Noman, 2015). Indulekha, (2017) (Otang and Afolayan, 2015) used two Citrus stated that the D- lemonine substance present in limon extracts (acetone and ethanol extracts) that the lemon peel is widely used in the food show a wide range of antibacterial activity in skin industry, it works to inhibit the microbial growth of diseases and a similar efficacy to synthetic the yeast during the fermentation process - antioxidants highlighting the medicinal value of therefore it must be removed before fermentation citrus limes as a potential source of drug - and pectin uses for thickening food products, development amid the apparent scarcity of gelling agent and stabilizer , also bioethanol can antiviral drugs For effective and safe bacteria, as be produced from peeling waste. well as validating the plant's ethnic treatment, they said that lemon showed great antibacterial and Health benefits of lemon antioxidant properties , so preventing health Lemon fruits are a rich source of vitamin C problems by enhancing nutrition. It also and flavonoids, and they are two antioxidants that significates treatment with the ethanol extract of work to remove free radicals in the cells of the Citrus limon exhibited restoration of the altered human body, thus protecting them from damage. biochemical parameters toward normal in Vitamin C is necessary for human health and an intoxicated rats. In the histopathologic studies, increase in the immune system, and its treated animals exhibited restoration of the liver deficiency leads to many health problems, the architecture toward normal (Bhavsar et al. 2007). early explorers knew this and took lemons on their The extract from lemon seed (Me OH) has potent long voyages to help prevent or treat scurvy. antioxidant activity and induces apoptosis cells, Regular eating of foods containing flavonoids leading to the inhibition of proliferation. These leads to protection from cancer and results suggest that aglycones and glucosides of cardiovascular diseases (Aedin et al. 2012). the and flavonoid present in extract Flavonoids also reduce the risk of stroke in may potentially serve as a chemo preventive women (Nicola et al. 2019). Studies have proven agent for breast cancer (Kim et al. 2012). In the use of lemon juice as a traditional treatment another study (Riaz et al. 2014) pointed out that for scurvy because it contains a high percentage Citrus limon possesses an anti-thrombin

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Salem et al. Importance of Lemon and future of its cultivation by using bio-fertilizers component and can prevent blood clots playing a and organic carbon increased. role in protecting the heart. Fresh lemon fruit is officially listed for use in Mode of action of bio-fertilizer plants and homeopathy in Germany. (According to The mechanism bio-fertilizers is through German Studies D for Homeopathic Medicines several biological processes like Nitrogen fixing 2019). Fresh lemon fruit can be effectively used to bacteria, mechanism of microorganisms to fix treat gingival bleeding and debilitating diseases. nitrogen is through the production of two types of Moreover, scientifically proven studies confirm metalloproteins that bind with the enzyme that contents of lemon fruits accelerate the nitrogenase and the production of N and NH3, regeneration of wounds in diabetics. (Murali and then the formation of ammonia (Bahat et al. Saravanan, 2012). In addition, studies have 2014). Microorganisms secrete a group of shown that the extracted from lemon organic acids and polysaccharides that contribute fruits has a significant anti-inflammatory effect to dissolving potassium compounds and making (Amorim et al. 2016), an anti-allergic effect them soluble by mineralization and thus be (Tsujiyama et al. 2013) and slimming properties absorbable from plants, as well as bacteria covert by reducing body weight and body fat mass (Kim insoluble phosphorus into soluble (Arti et al., et al. 2015). 2014) (Figure 4).

Type of Bio-fertilizers Bio-fertilization is biological preparation containing primarily plants strains of microorganisms in sufficient numbers, these microorganisms have definite beneficial roles in the fertility of soil rhizosphere and growth of plants.The multi strain bio-fertilizers might contains different strains of symbiotic associative diazatrophes, phosphate solubilizing microorganism, silicate dissolving microorganism, blue green algae and VAM (Saber, 1993a). Bio- Figure 4. Mechanisms of Plant Growth- fertilizers are products that contain huge numbers Promoting Rhizobacteria (Adopted from of cells of one or more types of beneficial García-Fraile et al. 2015). microorganisms for soil and plants alike, microorganisms that are usually used as a Bio-fertilizers effects on citrus growth component of bio- fertilizers are nitrogen fixes (N- Many vegetative growth characters (number fixers) and others that convert potassium (K- of shoots/one meter limb, shoot length and solubilizer) and phosphorus (P-solubilizer) into a thickness, number of leaves/shoot and leaf area) soluble form which the plant benefits and on orange trees were increased by using foliar encourages the vital balance in the soil., also they bio-fertilizers with NPK soil addition (Bakry et al. protect the environment as eco-friendly, and less 2013). Also, using bio-fertilizers showed that, of farms cost and increase income for the farmers. significantly increased growth plants such as fresh With using the bio-fertilizers and organic and dry weight of leaves, fresh and dry weight of fertilizers, can be helped achieving sustainability stem, plant height, plant diameter, number of sub of farms, minimizing the use of mineral fertilizers stems and flowers in lemon verbena (Mohammadi for non-depletion of raw materials and increase et al. 2013). Also, addition bio-fertilizers with their price, increasing soil fertility and maintain its organic and mineral fertilizers led to improvement natural structure, reducing concern about growth and the nutritional status of the Eureka environmental risks, increasing crop production to lemon trees (Ennab 2016). The growth of lemon provide food security (Akhtar and Siddiqui, 2009) seedlings was assessed in terms of seedling and improving the productivity of the trees (Saber, height, stem diameter, number of leaves, leaf 1993b).The addition of bio-fertilizers with chemical area, root growth, biomass accumulation, and bud resulted an increasing in the nitrogen content, take percentage, the high growth rate were available P and K in soil and increasing in organic observed with using bio-fertilizers (Patil, 2016). carbon and a difference in soil PH (Dixit and Gupta, 2000). (Ipsita and Singh, 2014) found that by adding bio-fertilizers, the soil's nutrient content

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Bio-fertilizers effects on treatment by using bio-fertilizers with doses of (yield) chemical fertilizers lead to increased physical and The addition of humic acid and bio-fertilizers biochemical characters of fruits.(Yogesh et al. in the soil for the purpose of treating root rot 2012). Sharaf et al. (2012) and Bakry et al. disease in resulted in a significant (2013) reported that, on Washington navel increase in the number of trees recovered and orange, the vegetative growth parameters and all greatly reduced the severity of the disease in the leaf macro elements content (N, P, K, Ca, Mg %) affected trees by inhibiting the pathogen's activity were increased significantly by addition bio & in the soil of treated trees, the treatment by bio- organic fertilizers as compared to control trees fertilizers also improved the yield and fruit quality (water sprayed). Also, trees product and fruit of the trees (El Mohamady and Ahmed, 2009). A quality was improved by addition bio-fertilizers. In study was carried out on eight years old the same context (El-Geuoshy, 2011) studied the Washington navel orange trees budded on sour effect of foliar spray with bio-fertilizers and he orange rootstock, the results indicated that trees revealed that the bio-fertilizers treatments treated with bio-fertilizers had remarked effect increased leaf photosynthetic pigments (canopy volume, leaf area, leaf dry weight and (chlorophyll A, B and carotenes) and leaf specific leaf weight, at the spring growth cycle) nutritional status on Navel orange trees. and increased leaf chlorophyll and mineral contents also achieved the best fruit yield and fruit CONCLUSION quality compared with untreated trees. Soil pH From the above discussion, it can be and salinity (EC) were decreased while available concluded that Lemon has many nutritional, macronutrients (N, P and K), soil microorganisms commercial and medicinal benefits, and its content was increased (Salama et al. 2017). cultivation must be taken into account, and bio- The main role of farmyard manure and bio- fertilizers are very important for vegetative growth, fertilizers with different doses of NPK was clear on yield and fruits quality for lemon trees, as well as Eureka lemon trees grown in sandy soil, for its importance with respect to soil and rebalancing supply nutrients which indispensable for the nutrients inside it, which stimulates growth in improvement of growth and the nutritional status addition to preserving the environment and of the trees and production of maximum yield with producing organic and clean fruits. a good quality. Also, farmyard manure and bio- fertilizers could compensate 50% of chemical CONFLICT OF INTEREST fertilizer without significant reduction in yield. This The authors declared that present study was treatment gave the best growth, yield, fruit quality performed in absence of any conflict of interest. and nutritional status of Eureka lemon trees. Besides, increasing soil content of most nutrients ACKNOWLEGEMENT without side harmful effects on the tree and The authors wish to acknowledge the financial environment (Ennab, 2016). For studying the support of Center for Research Excellence and influence of supplying Washington Navel orange Incubation Management (CREIM), Universiti trees with three sources of mineral nitrogen Sultan Zainal Abidin (UniSZA), Terengganu, (ammonium sulphate, ammonium nitrate and Malaysia. urea) with bio- fertilizers, it is found that bio- fertilizers with ammonium sulphate (2.43 kg/ AUTHOR CONTRIBUTIONS tree) amazing results on the amount of yield and Salem A., Wrote the manuscript; M. M. fruit quality, followed by using of bio-fertilizers with Khandaker, N. A. Badaluddin, U. A. Abdullah, K. ammonium nitrate and urea in descending order. S. Mohd, N. E. M. Shaari, and K. Mahmud, review (Mansour and Shaaban, 2007). and editing the manuscript.

Bio-fertilizer effects on citrus fruit quality Copyrights: © 2021@ author (s). In a study on sweet orange vc. Nuceller This is an open access article distributed under the confirmed that fertilizing with Azospirillum sp. and terms of the Creative Commons Attribution License PSB (as bio-fertilizers) alone or in combination (CC BY 4.0), which permits unrestricted use, with chemical fertilizers increased fruit quality and distribution, and reproduction in any medium, the biochemical parameters of sweet orange provided the original author(s) and source are fruits, among the treatments conducted in the credited and that the original publication in this study were the best results obtained was the

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