Round kumquat Citrus japonica, copyright Phuong Tran.

Belongs within: Citroideae.

Citrus is a genus of shrubs and small trees, many species of which are widely grown for their edible fruits. The taxonomy of this genus is particularly complex, with most cultivated taxa being of hybrid origin. Wild species are native to the Indo-Australian region with most cultivated varieties ultimately derived from Asian ancestors.

Are you sucking on a lemon or a lime?
Published 17 October 2008

The genus Citrus is one of the most significant groups of fruit trees around the world. An overwhelming diversity of fruit varieties are produced by Citrus, such as oranges, lemons, grapefruit, tangelos, citrons, bergamots, mandarins, and the wonderfully-named ugli fruit (and yes, it is). Technically, the fruit of Citrus is a specialised type of berry called a hesperidium, named after the mythical garden of the Hesperides where golden fruit were tended by airy nymphs watched over by a giant serpent, suggesting that Greek prophets had also predicted the eventual appearance of Benny Hill. The hesperidium is distinguished by its leathery, acidic rind and division into segments, and is unique to a clade containing Citrus and a few closely related genera such as Poncirus and Fortunella (kumquats*), both of which have been included by at least some researchers in Citrus (de Araújo et al. 2003). From the taxonomist’s point of view, however, Citrus has always been a gigantic headache. The question of how to classify this kaleidoscopic array of varieties, most of them only known as cultivated forms with no record of their origins, presents a quandary perhaps rivalled among plants only by the similarly over-cultivated genus Brassica. In the two main classifications that have been used for Citrus, that presented by Swingle in 1943 recognised sixteen species in the genus, while that of Tanaka in 1977 recognised one-hundred and sixty-two (Jung et al. 2005).

*Some time ago, I commented on the misleadingly obscene sound of words such as “yeast”, “moist” and “sphagnum”. None of these words, however, comes even close in this regard to the filth innocently suggested by “kumquat”.

The citrus variety known as poorman’s orange (it’s not an orange) or New Zealand grapefruit (it’s not a grapefruit, either). Photo by Julian Sauls.

As well as their long history of cultivation, citrus classification is also handicapped by the fact that the different varieties are at one and the same time both highly interfertile and significantly reproductively isolated. This may sound like something of a paradox, but it results from Citrus‘ distinctive reproductive system, involving a process called nucellar embryony (Moore 2001). The nucellus is the nutritive tissue surrounding and protecting the ovum in plant ovules. Seed development begins with the ovum being fertilised, and beginning to develop into an embryo. In Citrus, however, the nucellus itself also gives rise to a number of additional embryos that are genetic clones of the parent plant. These nucellar embryos often outcompete the sexually produced embryo, meaning that when the seed germinates the seedling that grows from it will commonly be genetically identical to its parent, and actual sexually-produced offspring are rare. In spite of this, actual direct barriers to reproduction between different species of Citrus are low, so when successful sexual reproduction does occur, the results can be unpredictable.

Kaffir lime Citrus hystrix, an ingredient that no good curry can do without. Photo from Trade Winds Fruit.

In light of the above, it is perhaps not that surprising that studies conducted on morphology and biochemistry of Citrus species in the 1970s came to the conclusion that of the 100+ potentially recognised species of cultivated Citrus, only three represented true “species” in the sense of deriving from separate domestications of independently evolved taxa. These three primordial species were the citron (Citrus medica), pummelo (Citrus maxima) and mandarin (Citrus reticulata). All other domestic “species” are ultimately derived from crosses, re-crosses and back-crosses of these three species and their derivatives. Oranges, for instance, are probably derived from hybrids of mandarins and pummelos, while the citron is an ancestor for lemons and limes. A fourth species, the uncultivated Citrus halimii, has also been suggested as a progenitor of cultivated varieties, but Pang et al. (2007) felt that it was not supported as such (apparently—I haven’t read the paper, as our library lacks the appropriate subscription). Nicolosi et al. (2000) added another species, the papeda Citrus micrantha, to the mix, representing the subgenus Papeda that includes Citrus micrantha and its close relatives such as the kaffir lime Citrus hystrix.

Probable relationships between citrus species, from Moore (2001).

I find it quite an impressive thought that the spectacular diversity of citrus fruits we see today should have come from so few progenitors. From pummelos to papedas to Poorman oranges, this is certainly something to keep in mind the next time you down a cocktail.

Systematics of Citrus

Characters (from Flora of China): Shrubs or small trees, evergreen, rarely deciduous. Young branches often flat and angled, usually with solitary (rarely paired) spines at axils. Leaves 1-foliolate, rarely 3-foliolate or simple; petiole usually articulated with base of leaf blade, usually conspicuously winged; leaf blade subleathery to leathery, with dense pellucid fragrant oil dots, margin crenulate or rarely entire. Flowers axillary, hermaphrodite or male, solitary or in small fascicles, fragrant. Calyx cup-shaped; lobes 3–5, subglabrous. Petals (3 or)4 or 5(–8), white or outside pinkish red, imbricate, thick. Stamens usually 4(–10)× as many as petals, free or basally coherent. Disk annular or short, with nectary glands. Ovary (3–)5–14(–18)-loculed, each locule with 2–8 or more ovules; stigma large. Fruit a berry (hesperidium) with sarcocarp segments of pulp vesicles and adaxially attached seeds. Seed coat smooth or ridged; embryo(s) 1 to many, like cotyledons milky white, green, or rarely yellowish, germination hypogeous.

|--C. aurantifoliaB00
|--C. aurantiumB00 [incl. C. vulgarisC55]
|--C. australasicaB00
|--C. australisB00
|--C. bergamiaR-CT01
|--C. decumanaC55
|--C. deliciosaR-CT01
|--C. demoruhocarpaDD73
|--C. garrawayaeB00
|--C. glaucaMS06
|--C. grandisA-G91
|--C. inodoraB00
|--C. japonicaMS06
|--C. javanicaC55
|--C. junosLO98
|--C. latifoliaCR01
|--C. limettaA-G91
|--C. limonB00
|--C. medicaA-G91
| |--C. m. var. medicaDD73
| `--C. m. var. acidaDD73
|--C. nobilisC55
|--C. paradisiB00
|--C. reshniCR01
|--C. reticulataB00
|--C. sinensisB00
`--C. tachibanaMH98

*Type species of generic name indicated


[A-G91] Al-Gboory, J. I. 1991. Biology of oriental citrus mite, Eutetranychus orientalis (Klein) on different citrus species. In: Dusbábek, F., & V. Bukva (eds) Modern Acarology: Proceedings of the VIII International Congress of Acarology, held in České Budĕjovice, Czechoslovakia, 6–11 August 1990 vol. 2 pp. 607–611. SPB Academic Publishing: The Hague.

Araújo, E. F. de, L. P. de Queiroz & M. A. Machado. 2003. What is Citrus? Taxonomic implications from a study of cp-DNA evolution in the tribe Citreae (Rutaceae subfamily Aurantioideae). Organisms Diversity & Evolution 3 (1): 55–62.

[B00] Braby, M. F. 2000. Butterflies of Australia: their identification, biology and distribution vol. 1. CSIRO Publishing: Collingwood (Victoria).

[C55] Candolle, A. de. 1855. Géographie Botanique Raisonée: Ou exposition des faits principaux et des lois concernant la distribution géographique des plantes de l’époque actuelle vol. 2. Librairie de Victor Masson: Paris.

[CR01] Chagas, C. M., V. Rossetti, A. Colariccio, O. Lovisolo, E. W. Kitajima & C. C. Childers. 2001. Brevipalpus mites (Acari: Tenuipalpidae) as vectors of plant viruses. In: Halliday, R. B., D. E. Walter, H. C. Proctor, R. A. Norton & M. J. Colloff (eds) Acarology: Proceedings of the 10th International Congress pp. 369–375. CSIRO Publishing: Melbourne.

[DD73] Deb, D. B., & R. M. Dutta. 1973. Contribution to the flora of Tirap Frontier Division. Journal of the Bombay Natural History Society 69 (3): 547–573.

Jung, Y.-H., H.-M. Kwon, S.-H. Kang, J.-H. Kang & S.-C. Kim. 2005. Investigation of the phylogenetic relationships within the genus Citrus (Rutaceae) and related species in Korea using plastid trnL-trnF sequences. Scientia Horticulturae 104 (2): 179–188.

[LO98] Lack, H. W., & H. Ohba. 1998. Die Xylothek des Chikusai Kato. Willdenowia 28: 263–276.

Moore, G. A. 2001. Oranges and lemons: clues to the taxonomy of Citrus from molecular markers. Trends in Genetics 17 (9): 536–540.

[MH98] Morikawa, H., A. Higaki, M. Nohno, M. Takahashi, M. Kamada, M. Nakata, G. Toyohara, Y. Okamura, K. Matsui, S. Kitani, K. Fujita, K. Irifune & N. Goshima. 1998. More than a 600-fold variation in nitrogen dioxide assimilation among 217 plant taxa. Plant, Cell and Environment 21: 180–190.

[MS06] Muellner, A. N., V. Savolainen, R. Samuel & M. W. Chase. 2006. The mahogany family “out-of-Africa”: divergence time estimation, global biogeographic patterns inferred from plastid rbcL DNA sequences, extant, and fossil distribution of diversity. Molecular Phylogenetics and Evolution 40 (1): 236–250.

Nicolosi, E., Z. N. Deng, A. Gentile, S. La Malfa, G. Continella & E. Tribulato. 2000. Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theoretical and Applied Genetics 100 (8): 1155–1166.

Pang, X.-M., C.-G. Hu & X.-X. Deng. 2007. Phylogenetic relationships within Citrus and its related genera as inferred from AFLP markers. Genetic Resources and Crop Evolution 54 (2): 429–436.

[R-CT01] Ragusa-di Chiara, S., & H. Tsolakis. 2001. Phytoseiid faunas of natural and agricultural ecosystems in Sicily. In: Halliday, R. B., D. E. Walter, H. C. Proctor, R. A. Norton & M. J. Colloff (eds) Acarology: Proceedings of the 10th International Congress pp. 522–529. CSIRO Publishing: Melbourne.

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