Are You Sucking on a Lemon or a Lime?

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.

REFERENCES

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.

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.

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

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.