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date: 23 March 2019

Citrus History, Taxonomy, Breeding, and Fruit Quality

Summary and Keywords

In May, every year since 1857, in the great park of Sans-Souci in Potsdam just outside Berlin—a park begun in 1745 by Emperor Frederick II of Hohenzollern and expanded a century later by Frederick William IV—the doors of the great Orangerie open in and a Renaissance-style garden called Sizilianischer Garten is set up. On horse-drawn carriages, large olive and citrus trees are brought outdoors, and are then raised in masters.

For the young European who, in the second half of the 18th century and in the first decades of the following, traveled to Italy to see and study Renaissance culture and the remains of Greek civilization, the citrus species and fruits and groves of southern Italy became the ultimate symbol of beauty and a sort of status symbol of wealth, particularly that of landowners. Nothing is more expressive of the fascination of their fruit than Abu-l-Hasan Ali’s 12th-century writings: “Come on, enjoy your harvested orange: happiness is present when it is present. / Welcome the cheeks of the branches, and welcome the stars of the trees! / It seems that the sky has lavished gold and that the earth has formed some shiny spheres.”

Indeed, Citrus spp. are among the most important crops and consumed fruit worldwide. Their co-evolution due to a millennial agricultural utilization resulted in a complexity of species and cultivated varieties derived by natural or induced mutations, crossing and breeding the “original” species (Citrus medica, Citrus maxima, Citrus reticulate, Fortunella japonica) and their main progenies (C. aurantium, C. sinensis, Citrus limon, Citrus paradisi, Citrus clementina, etc.). Citrus spread from the original tropical and subtropical regions of southeast Asia toward the Mediterranean countries of Europe and North Africa and, after 1492, in the Americas, not to mention South Africa and Australia, where they still have a very important role. Citrus species, wherever they have been cultivated, quickly became the protagonists of the letters and the arts, as well as the markets and gastronomy, and can even be found in religious ceremonies, such as for Feast of Tabernacles (Sukkot). Studies on Citrus botany, cultivation, and utilization have been pursued since the early stages of the fruit’s domestication and grew following their introduction in Europe, the Americas, Africa, and Australia. Citrus research involves many different aspects: such as the study of citrus origin and botanical classification; citrus growing, propagation, and orchard management; citrus fruit quality, utilization and industry; citrus gardening and ornamentals; citrus in arts and manufacturing.

Keywords: citron, mandarin, pummelo, water stress, alternate bearing

Introduction

Citrus include an important group of plants belonging to the Rutaceae family, subfamily Aurantioideae. Their commercial importance is enormous and their fruits, very rich in vitamin C, are not only consumed fresh but also transformed into juices, wedges, preserves, jellies, and jams, as well as providing by-products for cosmetic and medicinal uses.

The world of citrus fruits is so vast and complex that every aspect of their cultivation and culture could be, by itself, the subject of a whole volume.

Indeed, oranges and their derivatives are widespread and are consumed worldwide—to the tune of almost 70 million tons (MT) every year. Furthermore, fruit such as the citron (Citrus medica, Figure 1) have accompanied the development of agriculture since the dawn of the Indo-European civilization in Babylon, until they became an important part of the first great monotheistic religion, Judaism. In fact, every citrus fruit is a witness to eras and great civilizations and wherever they have been cultivated they have always aroused such wonder that they quickly became the protagonists of the letters and the arts, as well as the markets and gastronomy. Thus, orange is the very symbol of European Islamic agronomic knowledge and, at the same time, of delight, that spread throughout Andalusia and in Sicily at the turn of first millennium ce and in the following centuries. Citrus became, in some ways, the undying symbol of the Italian Renaissance, and, in particular, of the beauty of the Medici villas. The very idea of the Italian landscape, as a place of eternal spring, made immortal by Botticelli, not to mention Della Robbia sculptures and Bartolomeo Bimbi paintings, is well represented by the citrus. In all the great European courts, the fashion of orangeries became a necessity, and this tradition, albeit in a different way, continues with the fortune of ornamental citrus-growing in Italy.

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Figure 1. Citrus medica, cv Liscio di Diamante. P. Inglese.

The lemon (Citrus limon, Figure 2) had a similar fate: without it, the landscape of the Sorrento and Amalfi coast could not be imagined. In the 19th century, lemons from Sicily reached the markets around the world, when steam navigation replaced sails. Likewise the Mediterranean mandarin (Citrus reticulata, Figure 3), which conquered the Conca d’Oro valley of Palermo (Sicily) in the 19th century, and the clementine, which traveled from Algeria to Corsica to became familiar in all markets worldwide. This is without even mentioning some specificities, like the cultivation of bergamot (Citrus bergamia), whose products, perfumes, and teas (Earl Grey), are common to a large part of the world. Citrus fruit contribute so much to Italian culture and beauty, that any traveler would be still surprised with Stendhal, that “there is a country where orange trees grow in open fields? I asked the aunt ‘and having explained Aunt Elisabeth that there was this country and her name was Italia.’” In short, Citrus means a lot in so many countries, but none more so than Italy. The Washington Navel orange, for instance, was selected in Brazil, early in the 19th century, as a natural mutant of the blonde orange “Selecta,” and moved to Washington DC and then to Riverside in 1875 to became the most popular “navel” orange in the world.

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Figure 2. Citrus limon, cv Femminello. P. Inglese.

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Figure 3. Citrus reticulata, cv Tardivo di Ciaculli. P. Inglese.

History

The oldest quotation referring to citrus fruits is reported in the Chinese book Yu Gong that was written 4,000 years ago and recalls earlier documents. In one of them it is reported that during the reign of Emperor Da-Yu (21st century bce) a substantial tribute was established in the supply of some baskets with two types of citrus fruits: some small and some large, probably mandarins and pummelos. Indeed, citrus fruits were the subject of an offer, indicating they were considered fruits of high value.

Much later, in the year 304 ce, in the book entitled Plants of the southeast region of Chi-Han, citron which can be eaten with honey, sweet orange, and various types of mandarins are described. The Tachibana mandarin (C. tachibana (Mak.) Tan.) and the flat lemon Shiikuwasha (C. depressa Hay.) are considered native to southern Japan; they were present in wild form on the Ryukyu islands in southern Japan, as well as in the southwest part of the Japanese archipelago and in mountain areas of Taiwan.

The three-volume collection Ju Lu, written by Han Yanzhi in 1178 ce, represents the first specialized publication on citrus fruit. Inside there are 27 varieties of citrus, with detailed descriptions of mandarin, tangerine, sweet orange, bitter orange, lemon, trifoliate orange, and kumquat. For the first time, moreover, the cultivation techniques are illustrated, among with the nuclear selection, the preparation of cuttings, grafting, fertilization and irrigation of the soil, control of diseases and pests, and post-treatment collection.

In India many references to citrus fruits can also be found, especially to citron and lemon. Sacred writings in Sanskrit around the year 800 bce refer to them using the term jambila. In this language we meet the prefix nar, as a synonym of fragrance or perfume, which subsequently gave rise to the Arabic word narany.

Following the invasion of the satrapy of Media by Alexander the Great (356–323 bc), the botanists who followed his army knew the citron and its cultivation was widespread enough to give it the name of apple of Media (Malus medica) or apple of Persia (Malus persicae). The citron was introduced into Greece and then into Syria, Palestine, and Egypt. Indeed, more than 200 species are identified in the Bible, but not citrus fruits. The use of the citron fruits in the Feast of Tabernacles (Sukkot), following the rule given by the Lord to Moses (On the first day you will offer fruits of the most beautiful trees, palm leaves and leafy trees, Leviticus 23:40), began in the 2nd century bce, at the time of Simon Macabeo (143–134 bce), as reported by the historian Flavius Josephus (30–100 ce) in his work Antiquities of the Jews, in which he mentioned that, in order to acquire grace, one must “raise in his hands branches of myrtle, willow and palm trees, from which apples of Persia will hang,” that is, citrons.

Theophrastus of Ereso (327–288 bce) contemporary of Alexander the Great, in his Historia plantarum mentions the citron, saying that its fruits were not edible, but useful as an antidote against poison and to sweeten the breath. Dioscorides refers to the citron as medica mela or medica persica, suggesting its medicinal use. From Greece the citron moved to Rome; it was Virgil (70–19 bce) who was the first to mention it, in the Georgics, praising the fruit of the Media. Pliny the Elder (23–79) in his Naturalis historia initially called it malus assyria or medica and subsequently citrus, citrum, or citrea. He also stated that although the fruit was not edible, it was much appreciated and used for its medicinal virtues, especially against poisons, bad breath, stomach disorders, and the cravings of pregnant women. Marco Gavio Apicio, author of De re coquinaria, did not consider it from the alimentary point of view, from which it is likely that in Rome, during the 1st century ad, it was not used for this purpose.

It is not clear whether in the Roman Empire, in addition to the citron, lemon was known. In the excavations of Pompeii (Italy), more precisely in the Casa del Frutteto (1st century), paintings were found showing branches of lemons laden with fruit. The apparent resemblance between the plants and the fruits of the citron and of the lemon do not help in distinguishing them with certainty.

Citrus fruits spread throughout Europe as Islamism consolidated. Through the trade routes established from time immemorial, the bitter orange (narany) would have arrived from the East through Egypt and North Africa, in the Iberian Peninsula (al-Andalus) and in Sicily, Italy. We have news of its presence in the Middle East in the 9th century and in Andalusia (Spain) in the 10th century, as it is mentioned for the first time in an anonymous treatise of Andalusian agriculture. The earliest known citation of lemon (lamun) in Andalusia is due to Ibn Bassal of Toledo in his 11th-century Book of agriculture. Ugo Falcando in his Historia Hugonis Falcandi Siculi de rebus gestis in Siciliae regno described them as lumias (lemon). Ibn Luyun quotes lumias several times in his Treatise on agriculture (14th century) but did not provide any features that make it appear to be a different species (Citrus lime) from those known as lemon. The pummelo (zambua, istunbuti) was brought in Europe by the Arabs in the 11th century but it did not succeed. Regarding the lemon, Ibn Jamiya (1171–1193)—Salah al-Din’s (1138–1193) personal doctor—in his Lemon treatise described many of its virtues and a way to make lemonade. Also, the doctor and botanist of Malaga Ibn al-Baytar (1197–1248), in his Treatise on simple medicines, described the properties of lemon. It is worth nothing that for centuries the medicinal and ornamental uses of the fruits were much more important than the economic production for consumption. A new economic era began, with the use of sweet oranges for human consumption in Europe, after the Portuguese experienced these oranges in China. It was at the beginning of the 16th century when the first oranges arrived in the port of Lisbon through the route of the Cape of Good Hope. They were called oranges of Lisbon (Aurantium olysiponensis), according to the name of the arrival port, or “Portugal”; in the different European languages the sweet, blonde oranges are still named “Portugal” or “Portakal” or “Portekiz” in Turkish and البرتغال‎ (Portugal) in the Arabic spoken in North African countries (Figure 4). No citrus fruits, of course, arrived in America until 1492. Bartolomé de Las Casas (1489–1566), in his History of the Indies, reported that the citrus fruits were brought to the New World by Christopher Columbus on his second journey. On November 22, 1493, they landed in La Española (Haiti) and sowed everything they had brought from Spain, certainly the seeds of oranges, lemons, and citrons. The first orange trees that were established on the continent grew in Mexico in 1518, according to Diaz del Castillo (1495–1584) in his History of the conquest of the new Spain. The Jesuits, in the last third of the 16th century, spread citrus fruits across most of South America. Citrus arrived in Florida between 1513 and 1565, through the colonies of the Franciscan missionaries (Mission of St. Augustine). Rapidly, they spread to Georgia and South Carolina and later, starting in 1769, they were introduced to California by Spanish colonizers and missionaries who cultivated them in their gardens. The introduction to Brazil certainly took place between 1530 and 1540. But it was in the 19th century that the ornamental use of citrus gave way to the economic one, thanks to market demand for fruit, citric acid, and essential oils. New cultivars of sweet orange, lemon, and, later, mandarins were rapidly selected for the production of edible, commercial fruit and grafted in seedling rootstocks (C. aurantium, C. paradisi, C. lime, etc.). In 1837 the English botanist James Macfayden named the grapefruit (C. paradisi, Figure 5), the fruit that the naturalist Griffith Hughes had called the “forbidden fruit” in his Natural history of Barbados (1750). It was introduced in the Bay of Tampa, Florida, in 1823, and from there it spread to California and to the Mediterranean countries. In 1805 Sir Abraham Hume brought to England, from Canton, the common Mediterranean mandarin (C. deliciosa Ten.); lately, it was brought to Malta and diffused by the Botanical Garden of Palermo in 1804 (Figure 6). Specific cultivation techniques for intensive production were developed, considering the extraordinary economic value, particularly in southern Italy and Sicily. In Sicily, citrus growing, especially of lemon and mandarin, at the turn of the 19th and 20th centuries was regarded as a symbol of absolute wealth; the fruits’ value rose so highly that the construction of terraces to allow the cultivation of steeply sloping areas took off. In Spain, the first commercial orchards were planted at the end of the 18th century and in the 19th century citrus production became a market-oriented activity. From its introduction in California, in 1875, the Washington navel orange became a commercial phenomenon on a universal scale.

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Figure 4. Citrus chinensis, Blonde Oranges Sold on the Galata Bridge of Istanbul. P. Inglese.

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Figure 5. Citrus paradise cv Star Ruby. P. Inglese.

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Figure 6. Citrus reticulata, cv Avana. P. Inglese.

New varieties more pleasing to consumers were selected during the 20th century and citrus fruits are now grown in more than a hundred countries with tropical and subtropical climates, with a world production of around 100 MT per year.

Taxonomy, Evolution, and Breeding of Citrus

The genus Citrus belongs to the order of the Geraniales, family Rutaceae, subfamily Aurantioideae. The Rutaceae family includes about 160 genera and 1,650 species consisting of trees and shrubs. Diploid plants belonging to the genus Citrus have a haploid genome of about 367 Mb and 2n = 18 chromosomes. Citrus plants are evergreen and grow and produce fruits in quite different climatic conditions, at latitudes between 40° north (Corsica, Japan) and 40° south (New Zealand), from the warm/humid climates of the equator to the subtropical ones of the Mediterranean basin. On the basis of genomic, phylogenetic, and biogeographic analyses, scientists agree the primary centers of origin for the citrus species are the tropical and subtropical regions of southeast Asia, influenced by monsoons, the northeastern India at the Himalayan foothills, southwestern China (Yunnan province), Myanmar, the Indochinese peninsula, and the Malaysian archipelago, from which Citrus began the spread into the other continents. Recent analyses (Wu et al., 2018) suggest that the ancestral citrus species underwent a sudden speciation event during the late Miocene. Eventually, the Australian citrus species and the native Japanese Tachibana mandarin split from the mainland citrus during the early Pliocene and Pleistocene, respectively. Citrus domestication probably began with the identification and asexual propagation of selected, possibly hybrid or admixed, individuals, rather than recurrent selection from a breeding population as for annual crops. The genus Citrus is also a result of a long and complex domestication process and this, together with sexual compatibility between Citrus and related genera and the frequency of bud mutations, makes citrus taxonomy and phylogeny very complicated. Human selection, leading to development of most of the varieties we know, appeared much later. With Linnaeus, the classification of citrus species underwent an important turning point: in his work Genera plantarum, dated 1737, for the first time the genus Citrus and the three species belonging to it were named: Citrus medica, a species that included citrons and lemons, Citrus aurantium which included the sweet orange, the bitter orange, and the pummelo, and Citrus trifoliata, indicating the Poncirus. In Systema naturae, Linnaeus added the species Citrus decumana, indicating the pummelo that was thus separated from the orange. Thanks to the collaboration between Linnaeus and Osbeck new binomial names were introduced, including the pummelo (Citrus grandis (L.) Osbeck) and sweet orange (Citrus sinensis (L.) Osbeck), whose names have now been changed again (Figure 7). Indeed, numerous classification systems have been formulated, among which those of Swingle (1943) and Tanaka (1977) have been the most widely accepted. Swingle described 16 Citrus species while Tanaka described 162. Barrett and Rhodes (1976) suggested that there were only three true species within the cultivated Citrus and that all other genotypes derived from crosses between these true species. This concept has gained further support from various studies using nuclear DNA markers (Nicolosi et al., 2000).

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Figure 7. Citrus grandis, cv Goliath. P. Inglese.

The different types of citrus we know derive from three main taxa: the citron (Citrus medica L.), the pummelo (C. grandis (L.) Osb.), and the mandarin (C. reticulata Blanco). Natural selection, occasional hybrids, spontaneous mutations, apomixis account for the onset of most of the subsequent species that begun the spread of the Citrus in areas close to those of their origin.

In 1943, W. T. Swingle proposed a new system for the classification of Aurantioideae in The botany of citrus and its wild relatives. His classification is the one most commonly used in which two tribes are recognized, the Clauseneae and the Citreae. The first includes three subtribes and five genera considered primitive, Micromelum, Glycosmis, Clausena, Murraya and Merrillia; the second, larger and economically important, also divided into three subtribes, Triphasiinae, Citrinae, and Balsamocitrinae, includes 28 genera among which are the Citrus and the related genera Fortunella, Eremocitrus, Poncirus, Clymenia, and Microcitrus. Overall, the number of species belonging to the subfamily of Aurantioideae is over 200. In particular, the subtribe of the Citrinae—to which cultivated species of Citrus belong—includes 13 genera divided into three distinct groups according to the characteristics of the fruits:

  • Group A: primitive citrus fruits: Severinia, Pleiospermium, Burkillanthus, Limnocitrus, Hesperethusa.

  • Group B: fruits similar to citrus fruits: Atalantia and Citropsis.

  • Group C: real citrus fruits. This includes the genus Citrus and other five genera considered similar to it: Fortunella, Eremocitrus, Poncirus, Clymenia, and Microcitrus. The genus Fortunella includes four species: F. margarita (kumquat ovale), F. japonica (round kumquat), F. polyandra, and F. hindsii. The genus Poncirus consists of two species with the characteristic trifoliate leaves: P. trifoliata and P. polyandra. It is the only genus belonging to group C to have a species with deciduous leaves (P. trifoliate), a characteristic that makes it particularly resistant to low temperatures. Only one species, Eremocitrus glauca, belongs to the genus Eremocitrus. Native of desert areas of central-south Queensland in Australia, Eremocitrus is the only genus of the Aurantioideae family to have xerophytic habitus. The genus Microcitrus, according to Swingle, consists of six species: M. australis, M. australasica, M. inodora, M. garrowayii, M. maideniana, and M. warburgiana. The genus Citrus is divided into five groups of extremely significant economic importance: sweet oranges (C. sinensis (L.) Osbeck), mandarins (C. reticulata Blanco and C. unshiu Marc.), grapefruits (C. paradisi Macfadyen), lemons (C. limon (L.) Burmann f.), and lime (C. aurantifolia Christm. Swingle). Other species such as bitter orange (C. aurantium L.), pummelo (Citrus maxima Burm. or C. grandis (L.) Osbeck) and citron (C. medica L.) are less important from a commercial point of view, though the last two ones are at the origin of Citrus phylogenesis. The following are some characteristics of the main cultivated species.

    • Sweet orange (C. sinensis (L.) Osbeck) and bitter orange (C. aurantium L.), easily distinguishable by different morphological and sensory characteristics, have parallel origins: both derive from the cross between the pummelo, female parent, monoembryonic species, and the tangerine. The bitter orange (C. aurantium L.) came from the south of the Himalayas, from the northeast of India, and from Nepal, and the sweet orange (C. sinensis (L.) Osv.) from the northeast of India, southeast China, and Indochina.

    • Mandarins and mandarin-like cultivars. Mandarin is one of the three original species, progenitor of cultivated citrus, originated in the southeast of China. According to Swingle, the heterogeneous group of mandarins can be grouped into one species: C. reticulata Blanco. Clementine is a hybrid between a mandarin and sweet orange (Figure 8).

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      Figure 8. Citrus clementine, cv Common Clementine. P. Inglese.

    • Grapefruits and pummelos. The grapefruit, C. paradisi Macf., is the only autochthonous species of the New World. It is a hybrid derived from the natural cross between pummelo and sweet orange originating in the Caribbean Sea, probably in the Barbados islands. The pummelo (C. grandis (L.) Osbeck or C. maxima (Burm.) Merr.), original species, is a citrus fruit originated in southeast China, Indochina (Laos, Cambodia, and Vietnam), and Malaysia, and it is still very popular in China and various other Asian countries; the fruit is the largest among citrus fruit.

    • Lemons and citrons. From molecular studies it would seem that lemon, descending from citron and bitter orange, originated in northern India and probably in the southeast of China and northern Burma. The sweet lime (C. limettioides Tan.) comes from the archipelago of Southeast Asia and the hybrids between lemon and citron are numerous and widespread. The citron, C. medica L. is the third, very ancient, original species that originated in the northeast of India and Burma (Myanmar). Perhaps no fruit, like citron, has had so great an influence by religious rites in its diffusion. Citron took part in the origin of many citrus species, and cpDNA data indicate that citron always acted as the male parent. Indeed, bergamot (C. bergamia Risso and Poit.) and the Volkamer lemon (C. volkameriana Ten. and Pasq.) are both hybrids of bitter orange and citron; the wrinkled lemon (C. jambhiri Lush.) and the lime of Rangpur (C. limonia Osbeck) are both hybrids of citron and mandarin. Swingle gathers them in one species C. aurantifolia. The lime is commercially distinguished by sweet and sour and the latter by large and small fruit. Among the sweet limes (C. limettioides Tan.) the lime of Palestine is the most widespread: it derives from a cross between citron and sweet orange. Among the large-fruited bitter limes, C. latifolia Tan., the Tahiti lime, and the Bearss lime are more widespread. Among the small-fruited lime, C. aurantifolia (Christm) Swing., is the Mexican lime that is the most known and widespread; together with the alemow, C. macrophylla Wester, it is a hybrid of citron and C. micrantha, a species belonging to the subgenus Papeda.

The “genomic revolution” brought great innovation and shed light on the chaotic citrus taxonomy, based on long-standing, conflicting proposals, such as those of Swingle and Tanaka.

Citrus phylogeny has been investigated using Random Amplification of Polymorphic DNA (RAPD), Sequence Characterized Amplified Region (SCAR, and cpDNA Simple Sequence Repeats (SSR) markers, which, coupled with phylogenetic and biogeographic analyses, have very much enriched the knowledge on Citrus phylogeny and taxonomy, as well as that of the related Poncirus, Fortunella, Microcitrus, and Eremocitrus genera. A solid reformulation consistent with a full understanding of the hybrid and/or admixture nature of cultivated citrus species has been gained by several researchers, including Nicolosi et al. (2000) and Wu et al. (2018). Moreover, at the beginning of 2010, nucleotide sequences complete with two citron genotypes were deposited in public databases (Wu et al., 2018). A haploid line of Clementine was chosen by the International Citrus Genomic Consortium (ICGC) as the reference genome for all Citrus and sequenced with the whole genome shotgun method (http://www.phytozome.jgi.doe.gov). At the same time, a draft of the Ridge Pineapple variety of sweet orange was published, obtained using new generation sequencing methods. A Chinese research group has also sequenced a double haploid genotype of sweet orange, and tens of genotypes are underway. Obtaining complete information on the genomes of ancestral species and cultivated genotypes will be useful to understand the genetic basis of intra- and interspecific diversification and to identify the key genes that regulate numerous traits of agronomic interest. This information may be useful in the future to adopt more efficient genetic improvement programs.

The international market demands seedless fruit with good juice content, good organoleptic qualities (flavor, taste, sugar, acidity, etc.), easy peeling, and with an attractive appearance (size and color are very important in this context). Nutritional quality based on vitamin C, carotenoid, and polyphenol contents are considered as breeding criteria in some genetic improvement programs, together with disease resistance. In the Mediterranean region “mal secco” (dry disease) is probably the most important disease affecting lemons, and Alternaria is a problem for mandarin cultivars such as Fortune in Spain. Moreover, metabolomics studies concerns specific Huanglongbing (HLB or citrus greening), which is threatening close to 100 million trees worldwide, caused by Candidatus liberibacter asiaticus, a phloem-limited bacterium transmitted by psyllids, whose pathogenetic mechanisms of disease remain unclear. HLB is the most serious disease of sweet orange, mandarin, and grapefruit trees. It is destructive irrespective of rootstocks. The yield of affected trees is not only reduced considerably by continuous fruit drop, dieback, and tree stunting, but also by the poor quality of fruits that remain on the trees. It was estimated that the economic damage to the California citrus industry (45% of the U.S. citrus industry) due to citrus greening could range from $2.2 to $2.7 billion depending on orchard management (Lopez & Durborow, 2014).

Most of selected genotypes originated from spontaneous mutations, indicating the great importance of monitoring existing genotypes in modern citriculture. Mutations can be induced in order to produce limited changes in the original genotypes. This strategy was successfully applied in Israel and in the U.S., where new seedless-mutant mandarins were obtained (e.g., cultivars Mor and Tango) (Goldenberg et al., 2018). A relatively small number of genotypes of a certain commercial meaning originated from programs crossing and induced mutagenesis. Sexual breeding programs have a limited success in citrus genetic improvement because of the complex reproductive biology of these species (apomixis, sterility, incompatibility, juvenility, high heterozygosis levels). In particular for the tangerine-like type, the number of new individuals obtained through these techniques has increased considerably, also thanks to agronomic and technological innovations which allow efficient improvements and shortened times for the evaluation of new genotypes.

New rootstock genotypes have been obtained by sexual intergeneric hybridization between citrus species and Poncirus (Citrus trifoliate) or by somatic hybridization, but it is more difficult to obtain new scion genotypes. The selection of triploid lines is nowadays a breeding strategy of great promise, intended to obtain new seedless cultivars, as triploids are generally sterile. Several methods have been developed for triploid citrus creation, the most suitable are 2x X 2x crosses or interploidy crosses (4x X 2x or 2x X 4x). Biotechnologies, such as somaclonal variability, somatic hybridization, genetic transformation, and their integration with molecular biology tools (markers for early assisted selection and knowledge deriving from sequencing the entire haploid genome of citrus fruits; genome editing) in genetic improvement programs offer more and more rapid and efficient tools for the establishment of new genotypes that are more responsive to the changing demands of the consumer, especially in terms of the health and nutraceutical value of the fruit.

Citrus in Figures

The cultivation of citrus fruits worldwide has reached over 135 MT, more than half of which related to sweet orange. This production comes from an area of just under 9 million hectares (ha). China is the first citrus world producer with more than 30 MT, followed by Brazil with 21 MT, the U.S. with 12 MT, India with 8 MT, Mexico with 7 MT, Spain with 5.5 MT, and Italy with 3 MT.

The cultivation of citrus concerns a large number of countries and reveals a remarkable geographic dynamism, because the role of the different countries changes over time, above all due to the strong development of the sector occurred in Latin America (Brazil), and in Asia (China) in the last century and in the brief glimpse of the current one. Oranges (68 MT) account for almost 56% of citrus production, small fruits (mandarins, clementines, tangerines) (21 MT) 17.5%, lemons and limes (14 MT) 11.5%, and the other species (17.9 MT), the remaining 15%. Spain is the most important exporting country of fresh oranges, followed by Egypt, Morocco, South Africa, and the U.S. Strangely, the Netherlands is another orange-exporting country, although it does not have any production of its own. This fact is known as “commercial triangulation phenomena”: the country imports and then re-exports the same good. Mexico is the leading country for lime production, thanks to the growth of production since 2008. The European basin imports over 60% of the world’s total citrus export. Other currents are directed toward Asian countries (with a prominent position in Japan) and the Gulf area.

Spain

The cultivation of citrus fruits in Spain covers about 315,000 ha and is concentrated mainly (80%) along the coastal strip, the Levante river valleys and in the south of the Iberian peninsula (Andalusia), between 36.0º and 40.5º latitude N. Outside of these areas, and with some exceptions, the cultivation of citrus trees is very limited, due to the risk of frost. The new plantations are mainly found in the provinces of Huelva and Seville. In first decade of the 21st century, national production has settled on 6 MT. About half of this production (49%) is made up of oranges; mandarins and mandarin-like fruits account for 36%; while lemons account for only 4.5%. The production of other species is insignificant.

The “umbelicates” are the most widespread oranges and, among them, the Naveline cultivar is the most important, followed by the late ripening cultivar Lane late. Interest has been lost in Navelate, Washington navel, and Newhall cultivars, while the spread of Powell, Barnfield, Chislett, Fukumoto, Rohde is constantly increasing. Valencia late and other late varieties such as Barberina, Delta, and Midknight continue to spread, while Salustiana remains stable. Clemenules is the most widespread variety of mandarin, followed by others that ripen even earlier, such as Marisol, Oronules, and Clemenrubí, or later as Hernandina. Among the hybrids, Nova, Fortune, and Ortanique are the most important. Other mandarins, such as Nadorcott, are very welcome. The production of satsumas remains stable with the Okitsu and Owari varieties; the Iwasaki variety has spread, since the beginning of the 21st century. The production of lemons grows slowly; Fino is the most requested variety, followed by Verna.

China

In 2010, the total area under cultivation reached 2.21 million ha and production rose up to 26.45 MT, ranking second, after apples, in the ranking of the most cultivated fruit species in China. Citrus fruits are mainly grown in the tropical and subtropical regions between the 20st and the 33rd parallel north and between the 95th and the 122nd parallel east. Their cultivation in particular involves 19 provinces, with nine of them (Hunan, Guangdong, Fujian, Guangxi, Sichuan, Hubei, Zhejiang, Jiangxi, and Chongqing) contributing to 95% of the total national citrus production. Mandarin is the main species in China: in 2007 it represented 70.7% of total production, compared to 17% of sweet oranges, whose production reached almost 3.5 MT. Pomelo stood at 11%, while the share of the other citrus fruits (mainly kumquats and lemon) was 1.3%.

Brazil

Brazil is the world’s largest producer of oranges as well as orange juice and is by far the world’s largest exporter of orange juice. In 2010 Brazil produced 19 MT of oranges for a value of 3.7 billion USD (FAO STAT, 2010). Seventy percent of the oranges produced in Brazil are used by the processing industry. The United States Department of Agriculture (USDA) estimated the total production of orange juice (frozen concentrated orange juice, or FCOJ) in 2010–2011 at 1.47 MT (2009–2010: 1.095 MT). The remaining part of the crops (around 30%) satisfies the internal market for fresh produce. The export of fresh Brazilian oranges is small and marginal: worth USD 14.5 million for 31,800 tons (SECEX, 2011/2012), mainly shipped in the Netherlands, Spain and the U.K. Orange crops in Brazil cover around 800,000 ha (2012: 808,000—source: USDA). Brazil holds 53% of the world production of orange juice and 98% of total global juice exports. From 1962 to 2009 the Brazilian citrus industry has accumulated something like 60 billion in revenue from orange juice exports, with an average of 1.3 billion per year. Ninety percent of the Brazilian fruit juice market is represented by Europe and the U.S.

South Africa

South Africa ranks only 14th in world citrus production, producing about 2.3 MT of citrus (or 2% of world citrus production) in 2016. Yet South Africa ranks as the second largest exporter of fresh citrus in the world after Spain. Citrus production in South Africa has a strong fresh fruit export imperative: nearly 65% of the total crop is exported, ~20% is processed, and ~15% is consumed locally. Income from exports is ~90% of total citrus income. The citrus industry is the largest horticultural industry in South Africa in volume, and the second largest agricultural industry in value after the deciduous fruit industry. Approximately 32 million citrus trees or 58,000 ha of citrus are cultivated in South Africa.

The cultivar range in South Africa is composed by 69% sweet oranges (43% Valencia oranges, 24% navel oranges, and 0.5% midseason oranges), 14% grapefruit, 8% mandarins (2% satsuma mandarin, 4% clementine mandarin, 2% others), and 9% lemons (almost exclusively Eureka lemon). The greatest growth in the 1990s was in Star Ruby grapefruit, Midknight Valencia, and Delta Valencia oranges, and satsuma and clementine mandarins. In the late 1990s and early 2000s there was, in general, a planting slump mainly due to poor market performance; after this, increased plantings of Turkey Valencia and Cara Cara navel oranges, and late-maturing mandarins, occurred.

Italy

In Italy, citrus are cultivated on 137,468 ha, 58% of which are represented by oranges, 25% by clementines and mandarins, and 17% by lemons and other minor species (ISTAT, 2017). The cultivated areas are mainly located in southern Italy, particularly in Sicily, which is the national leader (57%), with 78,159 ha cultivated, followed at a considerable distance by Calabria (26%), with 35,829 ha invested. Citrus orchards are less popular in Apulia (6.8%), with 9,186 ha; Sardinia (4.8%); and Basilicata (4.2%). Most significant is the production of blood oranges (Tarocco, Moro, and their clones) and navel oranges designed with PDO, as well as the production of clementines in Calabria and lemons in Sicilian Syracuse province (Femminello Siracusano).

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Figure 9. Red Oranges, cv Tarocco. P. Inglese.

Fruit Quality and Post-Harvest Maintenance

Fruit Growth and Ripening

The citrus fruit is a berry called hesperidium, made up of different parts: exocarp (or flavedo), mesocarp (or albedo), and endocarp (carpel locule filled with juice). Citrus fruits have a very long growth period, ranging from six to over 12 months, depending on the species and varieties. In the northern hemisphere, the ripening calendar basically goes from July, with summer lemons, to late October with the earliest navel oranges until July for the latest Valencia oranges. Mandarins and mandarin-like fruits reach the market maturity from early October to April. Species and cultivars show a large variability of pre-harvest fruit drop. Late-ripening blond oranges such as Valencia Late maintain their quality characteristics almost unchanged for a long time (three to four months), while blood oranges are subject to a progressive deterioration.

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Figure 10. Juice made with Red Oranges. P. Inglese.

In general, growth, in terms of weight, follows a simple sigmoid pattern, with a more or less prolonged third phase, depending on fruit ripening time.

As for all non-climacteric fruits, the ripening process in citrus fruit takes place progressively and is interrupted when the fruit is removed from the plant. Thus, harvesting at the right degree of ripeness is important for storage. An extremely early harvest should be avoided, because it results in low-quality organoleptic characteristics, such as taste, color, and structure, as well as nutritional value. Even very late harvesting should be avoided, because the overripe fruits are delicate and easily subject to physiological disorders and post-harvest diseases. Overripe fruit show a sharp decrease in peel brightness, consistency, and essential oil content, accompanied by a decrease in juice acidity, whilst sugar content decreases at a slower rate. High transpiration rates also lead to rapid loss of firmness and juiciness.

Post-Harvest Maintenance

After harvest, a senescent process starts, characterized by a gradual decline of organic acids, vitamin C, sugars, and respiratory activity. Characteristic of the respiratory activity of citrus fruits is not homogeneous in all the parts that make up the fruit. In fact, it is higher in the flavedo compared to the albedo, and albedo compared to the endocarp. The sum of the respiratory activity of the skin, as a whole, is about ten times higher than that of the endocarp (Purvis, 1985). The respiratory activity, and consequently the post-harvest life span, is influenced by the skin features (consistency and thickness), specific weight, volume of flesh spaces (compactness of the segments, adherence of the endocarp to the peel, development of the cart cavity), and the succulence of the pulp. A fruit with thick peel, compact albedo, and adherent to the endocarp, in general has a longer post-harvest life than a fruit that has the opposite characteristics.

The relatively low metabolism that characterizes citrus fruits means that they have a sufficiently long shelf-life period. Experimental tests showed that citrus fruits do not benefit greatly from conservation in environments with concentrations of CO2 and O2 different from those normally present in the atmosphere, excluding the reduced severity of certain physiological disorders induced by low temperature storage, which nonetheless does not justify the use of controlled atmosphere conditions at commercial level. An environment saturated with humidity, on the contrary, reduces transpiration and slows down the processes of senescence. Water loss due to transpiration has been considered by many researchers the factor that most often affects the post-harvest life of citrus fruits, even more than the use of low temperatures of conservation (D’Aquino et al., 2017). In this context, individual fruit wrapping could be used for quality maintenance for the following reasons, when a plastic film highly permeable to gases is applied there is: (a) maintenance of quality even in uncontrolled temperature conditions for long periods; (b) improvement of gaseous exchanges due to the high surface developed by the film with respect to packaging in trays or cassettes; (c) reduction of cold damage in case of refrigerated storage; (d) the possibility to associate curing and/or substances with antimicrobial activity as an alternative to synthetic fungicides for protection against fungal attacks; (e) reduction of infections by pathogens for the barrier created by the film; (f) ease of removal of rotten fruits; and (g) better hygienic conditions and maintenance of healthy fruit even when in contact with rotten fruit.

Minimal processing (MPP) is very relevant in citrus since the fresh market is often limited by the inconvenience of peeling. Moreover, the fruit’s morphological characteristics make it suitable for MPP processing operations. Nevertheless, the operations involved in processing always reduces fruit shelf life since wounded tissues are more susceptible to pathogens’ growth than sound ones.

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Figure 11. Peeled Oranges and Mandarins Sold in a Street Market in Katmandu. P. Inglese.

Fruit Quality Parameters

The exocarp (flavedo) must be smooth, uniform in color (mostly due to carotenoids), relatively thin, and easy to separate from the segments. The flavedo is rich in pigments, essential oils, and vitamins; the spongy inner part of the peel (albedo) is rich in pectins, cellulose, flavonoids (hesperidin in oranges and naringin in grapefruits) and should not be thick and linked to the segments. The edible part of the fruit, the segments, develops from carpellar leaves, which are composed of multicellular vesicles filled with water and rich in organic acids (mostly citric acid), reduced sugars, pigments, and vitamins, as well as aromatic compounds. The stalk, which is surrounded by the segments, is present in fresh fruit and disappears after their senescence. Navel fruits contain a secondary fruit at their stylar end, which is covered by the epicarp of the main fruit. Most commercial citrus fruits are seedless due to parthenocarpy, but many mandarins, particularly in the Mediterranean region, and lemons, contain seeds. The most important index for the harvest is the ratio between total soluble solids and organic acids content (TSS/TTA). Harvest and quality parameters are specific for each species and cultivar. Commercial parameters for fruit quality include size, shape, minimal TSS/TTA and juice content (%), and an acceptable color. These traits change with species, cultivar, and country.

One of the main problems in achieving these quality standards is the high variability existing among fruit within the same tree or orchard, and changes occurring from season to season. This is particularly true for mandarins, which are very prone to alternate bearing, meaning trees yield small fruits in the “on” years. Prevailing light regimes and temperatures also affect fruit quality. Blood orange cultivars, like Tarocco, show an environmental effect in the extent of their pigmentation, because the development of the pigments (anthocyanins) that are dissolved in the cell sap is greatly affected by the prevailing temperatures, being higher in cool but not cold climates. Citrus fruits are rich in ascorbic acid, both in the epicarp and the juice (40–60 mg per 100 ml). Navel oranges may greatly differ in peel thickness and smoothness, being affected by poor irrigation and fertilization management.

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Figure 12. Excellent Uniformity of Selected Genova Lemons from Argentina. P. Inglese.

Research Needs and Highlights

Beside breeding, genetics, and disease control, the most important research areas related to citrus industry involve the development of new rootstocks, requested to tolerate diseases (Tristeza, HLB, etc.) and increase fruit yield and quality; the use of deficit irrigation to increase water use efficiency; the resistance to environmental stress, particularly soil salinity and nutrient deficiency; new strategies for orchard planting and, eventually, the control of alternate bearing that affects individual blocks, individual trees within a block, or even individual branches on a single tree in most citrus species. Indeed, a complex of factors such as poor flower bud differentiation in the “off” year, limitations in carbohydrate availability, hormonal balance, competition for nutrients, and changes in mineral status are responsible for alternate bearing of citrus cultivars. If biennial bearing results from the inability of branches to support flowering and vegetative shoot growth in the same year, it becomes imperative to maintain the balance between reproductive and vegetative growth year after year. The study of the role that some moderate level of environmental stresses, such as salinity or short-term low temperatures, may play on citrus physiology has revealed some beneficial aspects on citrus resistance to specific environmental conditions or on the increase of fruit yield and quality. For instance, a low salinity level may increase carbohydrate content in fruit, while moderate drought stresses may maximize flower induction, fruit formation, and retention, particularly in areas with very low or no chilling, although the magnitude of the drought stress has not been exactly specified. The growth of citrus trees has always required sophisticated irrigation systems that according to the ages and cultures have been conceived and built with the most diversified engineering solutions. Indeed, citrus have an indissoluble bond with water landscapes and water use efficiency. Water efficiency is greatly implemented by regulated deficit irrigation and there is a general consensus on micro irrigation (drip or micro sprinklers) being the most effective irrigation method for citrus growing. Micro irrigation allows water with nutrients (fertigation) to be supplied at very frequent intervals and couples this with a reduction of the amount of utilized irrigation water (Carr, 2012).

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Figure 13. Young Orange Orchard in Spain. P. Inglese.

Eventually, sustainability and resilience of citrus orchards are most important for growers and consumers. Wide ranges of C net ecosystem productivity in terms of C fixation in orchard systems may come from different strategies of orchard management. Net primary productivity (NPP) of an orange orchard reaches 5.5 tons C ha−1 year−1 in traditional and intensive systems, and the sustainability of the organic over the conventional system, both in terms of energy consumption and environmental impact, have been demonstrated (Liguori, Gugliuzza, & Inglese, 2009).

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Figure 14. Orange Blossom in Full Bloom. P. Inglese.

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