Citrus Mineral Nutrition and Health Benefits: A Review

Abstract

Citrus fruit is one of the most important fruits all over the world. Citrus fruits are essential sources of food and energy and play a critical role in supplementing healthy diets. They contain vitamins A, E, and B (thiamine, riboflavin, and niacin), minerals, and antioxidants such as flavonoids, vitamin C, phenolic compounds, and carotenoids as nutrients present in them. Mineral nutrients are essential nutrients found in many different types of plant and animal-based foods. Macro-minerals are required in large amounts while trace minerals are needed in minute quantities such as iron, zinc, and copper. Potassium is a vital nutrient in citrus fruit which regulates fruit size, fruit appearance, fruit color, and vitamin content. Fresh size and mass, percentage of rind and juice, soluble solids content (SS), titratable acidity (TA), SS/TA ratio, and industrial yield, expressed in kg of sugar per 100 kg of processed fruit or SS per box (40.8 kg) are used to evaluate fruit quality in citrus fruits. The amount of potassium below 0.4% affects tree development; otherwise, over an extensive range of variation does not generally affect plant growth. Potassium is one of the abundant elements in citrus fruits that affect both yield and quality. This chapter reviews the role of mineral nutrients in citrus production and the roles play in the human body.

1. Introduction

Citrus is a genus of evergreen tree or shrub that belongs to the family of Rutaceae and a native to the subtropical and tropical region of Asia [1]. There are several species of the genus citrus which include sweet orange (Citrus sinensis), mandarins (C. reticulata, C. clementina, C. deliciosa, C. unshiu and others), lemon (C. limon), limes (C. aurantifolia, C. latifolia, C. limettioides, C. limetta and others), grapefruit (C. paradisi), sour orange (C. aurantium) and shaddocks (C. grandis) [2, 3]. Citrus fruit is a very popular and important fruit that is cherished all over the world in the form of fruit salad, mixed salad, fruit juice, drink, and condiment in several kinds of preparations [4]. One-third of total citrus fruit production comes from orange juice production and this account for 80% of citrus fruit processing. The world production of oranges was estimated to be 76 million metric tons in 2019–2020, the largest producers were led by Brazil, China, India, the USA, Mexico, Spain, and Egypt [5]. Global citrus production reaches to 144 million metric tons in 2020. China ranking as the biggest producer of citrus followed by Brazil, India, Mexico, Spain, Egypt, Iran, and South Africa [5].

Mineral nutrients are essential for plant growth and development. They are the major class of food components necessary for the maintenance of physiological conditions that are essential for life [6, 7]. These essential nutrients are found in many different types of plant and animal-based foods. Mineral nutrients are classified into macro-minerals and trace elements. Macro-mineral is required in greater amounts and include calcium, potassium, sodium, phosphorus, magnesium, chloride, and sulfur whereas trace minerals are needed in smaller amounts, which may include iron, zinc, selenium, manganese, copper, iodine, cobalt, and fluoride. Both types of minerals support building, and maintaining healthy bones and teeth and also help to keep the muscles, heart, and brain working properly [8, 9]. Plants are the major sources of mineral elements in our diets; these substances are not synthesized in plants but are absorbed from the soil and the atmosphere. Therefore, the amount of minerals absorbed by the plants depends largely on the nutrient content and compositions of the soil where they were grown among other environmental factors [7, 10]. Additionally, nutrients play a significant role in soil fertility and make it more productive for plant growth [11]. Mineral nutrients required by citrus trees are in large quantities in order to attain adequate growth and yield, and the requirements for some of the nutrients vary with soil fertility and type.

Trace elements in fruit may be influenced by the amount of mineral composition of the soil, irrigation water, weather conditions, and the types and amounts of fertilizers used. There is a significant impact of fruit variety on mineral content [12, 13]. Trace metals in fruits are selectively accumulated and pineapple, for example, accumulated a high level of manganese as compared to other fruits studied [14]. The citrus pulp is recognized as providing some mineral elements such as potassium, calcium, phosphorus, or magnesium for human nutrition but there are other parts of the fruit that also contain these elements. The peels of orange, lime, and mandarin are not recognized in nutrition because they are non-edible components. But these peels of the fruits (orange, lime, and mandarin) like in their pulps are promising sources of mineral elements which can be used for their health properties in food products [15]. These properties can also be applied to food as a source of functional compounds [15].

2. Chemical composition of citrus fruits

Valuable natural chemicals in citrus fruits are an excellent source of different nutrients like carbohydrates, fiber, mineral elements, and vitamins required for the human body, including vitamins C, vitamins B, potassium, phosphorous, and other elements (Table 1). Citrus fruits contain an impressive list of other essential nutrients both glycaemic and non-glycaemic carbohydrates (sugar and fiber).

Component	C. Sinensis	Citrus paradisi	C. reticulate	C. aurantiifolia	Citrus aurantium	C. Limon
Moisture (g)	88.4	88.5	87.8	84.6	87.6	85
Protein (g)	0.8	1	0.9	1.5	0.7	1
Fat (g)	0.3	0.1	0.3	1	0.2	0.9
Fiber (g)	0.5	—	—	1.3	0.3	1.7
Carbohydrates (g)	9.3	10	10.6	10.9	10.9	11.1
Ash (g)	0.7	0.4	0.4	0.7	0.3	0.3
Calcium (mg)	40	30	50	90	26	70
Phosphorous	30	30	20	20	20	10
Iron (mg)	0.7	0.2	0.1	0.3	0.3	2.3
Thiamine (mg)	—	0.12	40	0.02	—	0.02 (in juice)
Riboflavin (mg)	—	0.02	—	0.03	—	0.01 (in juice)
Niacin (mg)	—	0.3	—	0.1	—	0.01(in juice)
Vitamin C (mg)	50	—	68	63	30	39 (in juice)
Carotene, μg	—	—	350	15	1104	—
Energy, K cal	43	45	—	59	48	57

Table 1.

Chemical composition of citrus fruits (per 100 g of edible portion) [16].

Vitamins A and E, B vitamins (thiamine, riboflavin, and niacin), minerals, and antioxidants such as flavonoids, vitamin C, phenolic compounds, and carotenoids are many nutrients present in citrus fruits. They also contain dietary fiber, which has a positive stimulatory effect on the immune system, cardiovascular, and digestive systems [17].

3. Potassium interaction with other nutrients

The positive effect between nutrients can be enhanced by the balanced application of two nutrients i.e. synergistic interaction. Antagonistic effects occur where an increase in one nutrient reduces the uptake and function of the other, thereby resulting in reduced crop quality. For example, the rate of Mg uptake can be depressed by Ca and vice versa [18]. This is due to higher affinity to Ca than to Mg in root plasma membrane binding sites [19]. The application of phosphorus is reported to reduce plant uptake and utilization of zinc [20, 21]. More so, an increase in the use of nitrogen fertilizer led to increasing in the uptake and utilization of zinc in plants [21]. Nitrogen and potassium in the fruits account for most of the nutrients removed from the soil by citrus trees each year and the interaction of K with N is considered the most important interaction. The process of converting inorganic nitrogen to organic nitrogen compounds is energy-consuming. Therefore, inorganic nitrogen absorbed by plants must be converted into amino acids and protein as much inorganic nitrogen is of no use to the plant. Good K nutrition favors the rapid turnover of inorganic nitrogen into proteins and consequently, potassium improves the effect of nitrogen fertilizer.

Mg uptake by the plant can be inhibited by the presence of high K concentrations in the soil and this may also induce Mg deficiency in plants [22]. K may also be reducing Ca uptake, where the soil is low or deficient in Ca despite the strong predominance of Ca on the exchange sites of the soils [23]. It is evident that K affects significantly the absorption and utilization of other nutrients by plants, and the appropriate K level differs in different crops.

K and N metabolism relationship has been evaluated in some studies. In contrast to the antagonistic relationship between K⁺ and NH₄⁺ nutrition, a positive correlation was found to exist between the acquisition rates of K⁺ and NO₃⁻ [24, 25] and the synthesis of amino acids and proteins can be enhanced by a sufficient supply of K, which promoted N metabolism [26, 27]. Potassium (K) deficiency was found to reduce Nitrate reductase (NR), Glutamine synthetase (GS), and Glutamate synthetase (GOGAT) activities and this inhibited nitrate absorption in certain plants [28]. More so, K deficiency was reported to up-regulate the activities of GS and Glucose dehydrogenase (GDH) in Arabidopsis [29]. The metabolism of N affected by K appears to vary in different types of plants. Meanwhile, the K concentration has a significant impact on C metabolism, and the metabolic process and energy level that exist between C metabolism and N metabolism show a strong interaction [30]. K supply of 6 mM to apple dwarf rootstock seedling was optimal; as it promoted photo-assimilate transport from leaves to roots and increased nitrogen use efficiency (NUE) which influences photosynthesis. This also enhances C and N metabolizing enzyme activities, nitrate assimilation gene activities, and nitrate transport [31].

4. Effect of deficiencies of mineral elements in citrus production

When plants are potassium (K) deficient, it affects the rate of photosynthesis. Nitrogen in large quantities with a little amount of K has resulted in having drops in protein used as building blocks, disease start setting up, reduction in carbohydrates production, reduction in fruiting, increasing fruit split, creasing of fruit, and drop in plugging. A decrease in yield and low fruit quality can be as a result of a shortage of K. Negative effects of low K generally occur on fruit yield and quality before leaf deficiency symptoms. K in the leaf range of 0.5–0.8% has been observed to have decreased yield and small fruit while K concentrations of 1.2% or more produced the maximum yield of high-quality fruit [32]. No visual deficiency symptoms were observed with moderately low concentrations of K in the tree which cause a general reduction in growth [32] and production is seriously impaired when there is an onset of visual deficiency symptoms in leaves.

Mineral deficiencies in certain plant may develop into leaf chlorosis symptoms. Different mineral deficiencies in citrus can result in distinct chlorosis patterns. Mg deficiency symptoms may appear as leaf interveinal chlorosis, with chlorotic development and necrotic lesion which occurs in later stages, particularly under high light intensity [33, 34]. Citrus trees with inadequate Mg may have no symptoms in the spring growth flush, but leaf symptoms develop as the leaves age and the fruit expand and mature in the summer and fall. Magnesium deficiency symptoms occur on mature leaves following the removal of Mg to satisfy fruit requirements.

Potassium-deficient plants as observed [35] do not develop leaf chlorosis but resulted in less biomass and some changes in nitrogen metabolism. The result of the experiment also shows that magnesium deficiency produced leaf chlorosis symptoms and loss of chlorophyll in the leaf. Reduction in nitrate concentrations brought about a partial impairment of the nitrate reductase system and this is due to effects on nitrogen metabolism [35].

Calcium deficiency was the only treatment that revealed profound effects on the nitrogen economy of citrus leaves. Remarkable lower nitrogen level in leaves and reduced nitrate concentration was observed in calcium deficient [35]. Calcium deficiency with nitrogen metabolism interference resulted in an extreme reduction of the free amino acid pool. The most abundant free amino acid in citrus is proline [36] and glutamic acids, the precursor of proline synthesis were most severely affected [37]. More so, a change in the protein level of Ca-deficient leaves might be caused by the decline in the level of ribulose bisphosphate carboxylase (RuBPcase) [35]. High concentrations of NH₄⁺, K⁺, Ca²⁺, Mn²⁺, and SO₄²⁻ in the soil can induce magnesium deficiency [38]. The uptake of Mg, Ca, and other cations by the citrus plant are usually interfered with by the high concentration of potassium (K) available in the soil either due to excessive use of fertilizer or natural soil minerals [39].

5. Mineral element as a factor influencing quality of fruits in citrus production

Inadequate mineral nutrition, whether due to deficiency or excess, may generate poor fruit quality. Therefore, it is necessary to achieve nutritional balance, in order to allow plants to grow vigorously and better tolerate biotic and abiotic stresses. Fresh size and mass, percentage of rind and juice, soluble solids content (SS), titratable acidity (TA), SS/TA ratio, and industrial yield, expressed in kg of sugar per 100 kg of processed fruit or SS per box (40.8 kg) are usually used to evaluate fruit quality in citrus fruits.

Nitrogen, phosphorus, and potassium are the most important nutrients that influence fruit quality of citrus fruits. However, deficiency or excesses in other nutrients have negative effects on fruit yield and quality [40]. Nitrogen (N) increases juice content, total soluble solid (TSS) per box and per acre, and acid content. However, excessive N can induce excess vigor and promote a vegetative rather than a flowering tree, and this can result in lower yields with lower TSS per acre. In contrast, poor fruit yields are produced when there is a low N level but promoted extensive flowering. Soluble solids: acid ratio increased with phosphorus but acid content reduced [40]. Fruit production, fruit size, green fruit, and peel thickness of citrus fruits are increased with potassium. Foliar spray of potassium nitrate or monopotassium phosphate in the spring often increases the fruit size of tangerine and grapefruit, and the fruit size and total pound solids of Valencia orange [40]. The use of urea can increase flowering and fruit set by foliar application (from 6 to 8 weeks before bloom) [40].

Productivity in low-fertility tropical soils can be enhanced by the use of fertilizer and this supports adequate mineral nutrition of citrus. Nitrogen (N) and potassium (K) fertilizers to some extent produce an increase in fruit yield and quality of citrus trees [41, 42]. Potassium also affects external fruit characteristics, in such a way that as the K supply increases, fruits become larger and coarse. But, K deficiency resulted in a reduction in the number and size of fruit in all citrus varieties and the soluble solids content of juice also decrease [42].

Citrus fruit requires high mineral nutrient amounts in order to express their full growth, yield, and fruit quality potential. In some cases, soil mineral concentrations are at sufficiency levels. However, it is necessary to apply acidity correctives for nutrients to become available and be used by the plant. The main macronutrient effects observed on citrus fruit quality include; an increase in juice color intensity, soluble solid (SS) and titratable acidity (TA), rind thickness increases, and color for nitrogen (N) [43]. They also observed reduction in titratable acidity and phosphorus (P) increases SS/TA ratio; potassium decreases SS, SS/TA ratio and juice color; while Mg was reported to have slight SS, SS/TA ratio, fruit fresh mass, and size increase and reduced rind thickness [43]. However, there is a need to validate these statements as citrus fruit quality is the product of complex actions that involved several factors, acting individually or together.

6. Roles of potassium in citrus production

Potassium (K) alongside nitrogen is one of the most important nutrients for citrus production. It is needed for enzyme activation, cell division, photosynthesis, photosynthate transport, and osmoregulation. Potassium is required in more quantities in the meristematic tissues, buds, leaves, and root tips of citrus plants [44]. It plays important role in maintaining an anion-cation balance in cells, involved in protein synthesis, opening and closing of stomata, activation of enzymes, and in the turgidity of cells [45]. Potassium regulates the value of fruits through its influence on the size of the fruit, appearance of the fruit, fruit color, and vitamin contents [46].

This important nutrient plays a key role in stimulating photosynthesis, maintaining rapid root growth, and synthesis of protein from amino acids [47]. It helps to keep the stability of electric charges - an essential for ATP formation in plant chloroplasts. Stability in pH will counterbalance the insoluble and soluble macromolecular anions by the application of a large quantity of potassium. A wide range of potassium content in the leaves is required for the average vegetative growth of citrus plants [48]. The amount of K below 0.4% affects tree development; otherwise, over an extensive range of variation does not generally affect tree growth [49].

Potassium (K) is the most abundant inorganic cation and is key in ensuring optimal plant growth [50]. K is an activator of dozens of important enzymes, such as protein synthesis, sugar transport, nitrogen and carbon metabolism, and photosynthesis. It plays an important role in the formation of yield and quality improvement [51, 52]. K is also very important for cell growth, which is an important process for the function and development of plants [44]. K has strong mobility in plants, helps in regulating cell osmotic pressure, and balances the cations and anions in the cytoplasm [45, 53]. Through these processes, K is involved in the regulation of stomata opening and closing, cell elongation, and other important physiological processes.

The effects of K level on plant growth have been studied by many scientists. K applied to Red Fuji apple with 600 kg/ha K produces the highest yield and fruit quality [54]. More so, the application of 6 mM K promoted pear growth and improved photosynthetic efficiency [55]. Treatment of potassium with 500 kg/ha resulted in increased production of navel oranges with better fruit and quality parameters [56]. Potassium interacts with other nutrient ions. Magnesium (Mg) uptake in the soil is inhibited by high concentrations of K and this may lead to Mg deficiency in plants [22]. Some fruit disorders are likely to occur under low potassium conditions or high leaf N: K ratios, like plugging and creasing, and these result in less marketable fruit.

Potassium (K) has a significant role in juice acidity properties. High K concentration increases juice acidity, while a low K concentration causes a decrease in juice acidity properties. High K availability in the soil can reduce the uptake of magnesium, calcium, and ammonium for plants [42]. Nitrogen (N) and potassium (K) in the fruits are the most nutrients removed from the soil by citrus trees each year [42]. The roles played by potassium in the plant may include; root growth enhancement, drought tolerance, decreasing water loss and wilting, improving pest and disease resistance, and reducing stalk lodging [57]. Plants required potassium in the range of 0.5 to 2% of dry matter, which is next to that of nitrogen. When the K level is in the ideal range, then a satisfactory yield of fresh fruit can be attained.

6.1 General guidelines in potassium application

Potassium is more taken up by citrus fruits than any other nutrients. Potassium application rates can be done either upon a leaf or soil analysis but soil analysis is the most commonly used one. Potassium (also called potash) is listed on the fertilizer label as K₂O and application rates of 0.8–1.4 lb. K₂O/tree are commonly used in 3–5 splits during the growing season [58]. During late fruit growth, potassium uptake usually occurred and application rates should be increased to meet this need (Table 2).

Flowering	Establish good early growth
Fruit set	Continued strong growth
Fruit enlargement and maturation	Maximize fruit fill and fruit size, productivity, skin quality, and vitamin C content and reduce granulation and fruit splitting
Post harvest	Maintain long-term fruit productivity

Table 2.

Potassium at citrus growth stages [58].

7. Roles of mineral nutrients in human consumption of citrus fruits

7.1 Roles of potassium and sodium in citrus fruits

Citrus fruits are good sources of potassium. An orange may provide 6% of the dietary reference intake (DRI) of potassium, while a glass of orange juice provides 10% of the DRI [59]. Potassium played an important role in regulating water, electrolyte balance, and acid–base balance in the body [59, 60]. In addition to potassium, sodium is also responsible for the regulation of water and electrolyte balance. A glass of chilled orange juice or a few fresh oranges/mandarins is very refreshing in summer and also provides the required electrolytes.

Citrus fruits contain much less amount of sodium than potassium, which is important to patients with high blood pressure regulation, a condition associated with hypertension [59]. Orange has been reported to contain more potassium than any other citrus fruit [61]. An important property of fresh citrus fruits is their low energy value, negligible sodium concentration, and their replacement by potassium, which may be important for low-fat and restricted diets. Potassium in citrus fruits enhances the normal functioning of muscles and the nervous system in the body. Without this essential mineral, the impulse to signal the body to move could not be possible. It helps in the contraction and flexing of the muscles in the heart and other organs [8].

Potassium is the most abundant mineral of citrus juices and accounts for 40 percent of the total ash content [62]. Citrus fruits are low in sodium with a value relatively low (3–4 mg/178 ml orange juice and 4.5 mg/178 ml tangerine juice) [63]. Potassium content between 4 to 6 meq is available in 100 ml of orange juice [59]. Potassium contents in orange, grapefruit, and tangerine were reported to be 237, 350, and 132 mg, respectively [64]. Potassium intake can be increased by consuming citrus fruits and juices. One medium orange and one 225 ml of a glass of orange juice provide approximately 235 and 500 mg of potassium respectively [65]. These two elements are the main cations of the cell and persons with high blood pressure are usually placed on a low-sodium diet. Although potassium deficiency in normal adults is rare, people on diuretic medicine or on an improper diet have been known to need a supplemented intake of this element. The study of the researchers had confirmed that citrus fruits (oranges and pomelos) are not a rich source of sodium [66], therefore can be used in diets for people with cardiac or kidney problems or those susceptible to osteoporosis [67, 68, 69].

7.2 Roles of calcium, magnesium, and phosphorus in citrus fruit

Calcium and magnesium are the two major divalent cations of citrus fruit. These cations are found between 8 and 15 mg/100 ml in orange, tangerine, and grapefruit juices [63]. These two mineral nutrients contributed 2–3 percent U.S. RDA per serving of 177 ml in citrus juices. Phosphorus is a bivalent cation present in the blood cells as phosphates, in protein, lipids, and carbohydrates, and in adenosine triphosphate and adenosine diphosphate (ATP and ADP). The U.S. RDA for phosphorus is 1 g; orange juice and grapefruit juice contain between 14 to 20 mg per 100 ml of phosphorus [63]. Citrus fruits compared to other fruits, such as apples, pears, melons, peaches, plums, mangoes, and bananas, are a valuable source of calcium, which plays an important role in building hard, strong bones [59].

The citric acid in orange juice may act as a chelating agent and thus increase calcium absorption by preventing the formation of insoluble salts. They are also a valuable source of phosphorus, which together with calcium, participates in the formation of strong bones and teeth [70]. Pulp from one pomelo fruit (about 600 g) provides 9 to 16% of the DRI for phosphorus while the rind (about 320 g) also provides about 30–40% less of the DRI for phosphorus than the pulp [71]. Phosphorus is important in the diet of young people, pregnant and lactating women. Plant seeds (beans, peas, cereals, and nuts) and fruits contain phytic acid (also called phytate), that is not directly available to humans [71]. Phosphorus in citrus fruit is an essential element in the building blocks of life; the ribonucleic acids (RNA), which is required for many additional biochemical and physiological processes that include energy transfer, protein metabolism, and other functions [72]. Calcium is highly implicated in the maintenance of firmness of citrus fruits [73] and its requirements in fruits are related to cell wall stability and membrane integrity [74]. Magnesium is an important primary constituent of chlorophyll and as a structural component of ribosomes, which helps in their configuration for protein synthesis [75]. It is also required for the maximum activity of almost all phosphorylating enzymes in carbohydrate metabolism.

7.3 The roles of copper, zinc, iron, and manganese in citrus fruits

Trace metals (copper, zinc, iron, manganese, etc) are needed in the body in a small or minute quantity. These plant nutrients are supplied in citrus fruit during their cultivation. They are important in many metabolic activities of the body. Iron content in one orange (200 g) can provide about 2 mg of iron. Two oranges a day can give 4 mg, which would be more than 10% of the Recommended Dietary Allowance (RDA) in the USA. The RDA is set assuming a 10% rate of intestinal absorption [76, 77].

Oranges and pomelos are the fruits richest in iron and copper, they could be recommended in cases such as hemoglobin production disorders resulting from a deficiency of these elements [61]. Pineapple contains copper, which regulates the heart rate and blood pressure [78]. Manganese in pineapple juice help to build strong bones, connecting tissues in the body and boosting the immune system [79]. A person can get rid of nausea, constipation, throat infections, and intestinal worms by consuming pineapple juice [79]. An equally important micronutrient is zinc, which protects the body against oxidative stress and stimulates immune mechanisms [80]. Its content in the peel of orange, lemon, and all grapefruit varieties was found to be significantly higher than in the pulp [61]. Cereals and vegetable diets contain phytates and these phytates inhibit zinc and calcium absorption supplied in citrus fruits therefore caution should be taken in consuming citrus fruits along with cereals and vegetables.

8. Conclusion

Citrus fruit is an evergreen tree that needs all the essential nutrients for proper metabolic functioning. A balance between macronutrients and micronutrients is needed to optimize the yield of high-quality fruit and maintain healthy trees that are tolerant to pests, diseases, and other unfavorable conditions. Citrus fruits are valuable sources of potassium, which is needed to ensure water and electrolyte balance in the body. More so, increase consumption of citrus fruits and products provide virtually all the mineral elements needed by the body to maintain good health and prevention of degenerated diseases.

Conflict of interest

The authors declare no conflict of interest.