Citrus taxonomy

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botanical classification
of the species, hybrids, varieties and cultivars belonging to the genus Citrus is called "citrus taxonomy".

Citrus taxonomy refers to the

cultivars, and graft hybrids within the genus Citrus
and related genera, found in cultivation and in the wild.

Citrus taxonomy is complex and controversial.

bud mutation.[6]

Detailed genomic analysis of wild and domesticated citrus cultivars has suggested that the progenitor of modern citrus species expanded out of the Himalayan foothills in a rapid radiation that has produced at least 11 wild species in South and East Asia and Australia, with more than a half-dozen additional candidates for which either insufficient characterization prevents definitive species designation, or there is a lack of consensus for their placement within the Citrus genus rather than sister genera. Most commercial cultivars are the product of hybridization among these wild species, with most coming from crosses involving citrons, mandarins and pomelos.[7][8] Many different phylogenies for the non-hybrid citrus have been proposed,[9] and the phylogeny based on their nuclear genome does not match that derived from their chloroplast DNA, probably a consequence of the rapid initial divergence.[7] Taxonomic terminology is not yet settled.

Most hybrids express different ancestral traits when planted from seeds (

nucellar seeds in a process called apomixis.[4]
As such, many hybrid species represent the clonal progeny of a single original F1 cross, though others combine fruit with similar characteristics that have arisen from distinct crosses.

Genetic history

Highest-probability phylogenetic branching of pure citrus species (Wu, 2018; Wu, 2021)[7][8][10]
ichang papeda
common mandarin
Ryukyu mandarin
desert lime
finger lime
round lime
kumquat
micrantha
citron
pomelo
mangshanyegan

All of the wild 'pure' citrus species trace to a common ancestor that lived in the Himalayan foothills, where a late-

mangshanyegan (C. mangshanensis), and the oval (Nagami) kumquat (Fortunella margarita or C. japonica var. margarita). Three from Australia were identified: the desert lime (C. glauca), round lime (C. australis) and the finger lime (C. australasica). Many other cultivars previously identified as species were found to be closely related variants (subspecies or varieties) or hybrids of these species,[7] though not all cultivars were evaluated.[10] Subsequent studies have added two additional species to this list of pure species: a mandarin native to the Ryukyu Islands designated C. ryukyuensis,[8] and a rare wild species from Southeast Asia, the mountain citron.[12] A number of further species originally placed in other genera have recently been subsumed into Citrus as a result of phylogenetic analysis, but these have yet to be characterized on a phylogenomic level to confirm their status as unique pure species.[13]

Artificial interbreeding seems possible among all citrus plants, though there are certain limitations to natural interbreeding due to plant physiology and differences in natural breeding seasons. This ability to cross-pollinate extends to some related species that some classifications place in distinct genera. The ability of

southern China, and Japan.[14] The hybrids of these taxa include familiar citrus fruits like oranges, grapefruit, lemons, and some limes and tangerines.[1][15] These three have also been hybridized with other citrus taxa, for example, the Key lime arose from a citron crossing with a micrantha.[7] In many cases, the varieties are propagated asexually
, and lose their characteristic traits if bred. Some of the hybrids have in turn interbred with one another hybrid or with the original taxa, making the citrus family tree a complicated network.

Ternary diagram of hybrids of the three major ancestral species. Data from Curk et al. (2016).[16]

finger lime and calamansi
cross).

Citrus naming systems

See also: Botanical name
See also: Hort.

Initially, many citrus types were identified and named by individual taxonomists, resulting in a large number of identified species: 870 by a 1969 count.[18] Some order was brought to citrus taxonomy by two unified classification schemes, those of Chōzaburō Tanaka and Walter Tennyson Swingle, that can be viewed as extreme alternative visions of the genus.[18][7]

Swingle's system divided the Citrinae subtribe into three groups, the 'primitive citrus' distant relatives, the closer 'near citrus' including citrus-related genera like Atalantia, and the "true citrus", for the species that had historically been placed in Citrus but many of which he elevated to separate genera: Poncirus (trifoliate orange), Fortunella (kumquat), Eremocitrus (desert limes), Microcitrus (finger and round limes), as well as an additional genus, Clymenia, formerly thought to be a citrus hybrid. His Citrus he likewise subdivided into two subgenera: citrons, pomelos, mandarins, oranges, grapefruits and lemons were placed in subgenus Eucitrus (later called simply subgenus Citrus), while the hardy but slow-growing trees with relatively unpalatable fruit he placed in subgenus Papeda.[19][20][21] His genus Citrus consisted of just 16 species, dividing them further into varieties, and lastly cultivars or hybrids. The Swingle system is generally followed globally today with much modification; there are still large differences in nomenclature between countries and individual scientists.[22]

The 'Tanaka system' (1954) instead provides a separate species name for each cultivar, regardless of whether it is pure or a hybrid of two or more species or varieties, and resulted in 159 identified species.[18] It thus represents an example of taxonomic "splitting",[23] and in assigning separate species names to horticultural variants does not conform to the standard species concept.[18] Tanaka also divided into subgenera, but different than in Swingle's system, introducing Archicitrus (which he subdivided into five sections, Papeda, Limonellus, Aruntium, Citrophorum and Cephalocitrus) and Metacitrus (divided into Osmocitrus, Acrumen and Pseudofortunella).[20][24] This system is commonly used in Tanaka's native Japan. A 1969 analysis by Hodgson intended to harmonize the two schemes accepted 36 species.[18][21]

These initial attempts at Citrus systematization all predated the recognition, which began to gain traction in the mid-1970s, that the majority of cultivars represent hybrids of just three species, citron, mandarin and pomelo.

Feroniella.[27][28] There remains a lack of consensus as to which wild plants and hybrids merit distinct species status, a phenomenon exacerbated by the prior failure to correctly identify the genetically pure citrus strains and distinguish them from hybrids.[7]

Ollitrault, Curk and Krueger system of hybrid citrus species names. Not all possible combinations are known to exist.

In 2020, a new taxonomic system was proposed by Ollitrault, Curk and Krueger, with the goal of harmonizing traditional naming systems with the new genomic data that have both allowed the pure ancestral species to be distinguished from hybrids, and enabled the ancestry of those hybrids to be identified among the ancestral species. In their system, each ancestral species has a binomial name, while a unique species name is reserved for each combination of ancestral species, independent of the specific order of crossing or proportional representation of the ancestral species in a given hybrid.

Individual hybrids of each type are then distinguished by a variety name. Thus hybrids that are crosses between mandarin (C. reticulata) and pomelo (C. maxima) would all be C. × aurantium, with specific crosses including: C. × aurantium var. sinensis for the sweet orange, C. × aurantium var. paradisi for grapefruit, and C. × aurantium var. clementina for the clementine. Likewise, hybrids combining mandarins and citrons would all be varieties of C. × limonia, those of pomelo and citron, C. x lumia, while tri-species hybrids of citrons, pomelos and mandarins would be C. × limon, and a tetra-species cross involving these three species along with C. micrantha would be C. × latifolia.

This naming system focused on the four species ancestral to most commercial hybrids, and did not include similar species designations for more exotic hybrids involving other citrus species, such as the Ichang papeda, kumquat, or trifoliate orange. Likewise, Ollitrault, Curk and Krueger accepted that the whole-genome characterization necessary to unambiguously assign a hybrid species name under their system is not available for many varieties.[13]

Core species and hybrids

See also: Folk taxonomy
Examples of hybrid Citrus, showing their derivation from the pure founder species

Most commercial varieties are descended from one or more of the 'core species',

bud sports, clonal families of cultivars that have arisen from distinct spontaneous mutations of a single hybrid ancestor.[7][14] Novel varieties, and in particular seedless or reduced-seed varieties, have also been generated from these unique hybrid ancestral lines using gamma irradiation of budwood to induce mutations.[29]

Ancestral species

Mandarins

Mandarin oranges (tangerines, satsumas – Citrus reticulata) are one of the basic species, but the name mandarin is also used more generally for all small, easily peeled citrus, including a large range of hybrids.[30] Swingle saw three species of mandarin, while Tanaka identified five groups with a total of 36 species. Webber (1948) divided them into four groups, king, satsuma, mandarin, and tangerine, and Hodgson (1967) saw in them four species.[7][30] Genomic analysis suggests just one mainland-Asian species, Citrus reticulata.

In an observation originally made in a study of their hybrid progeny, a subspecies-level division has been characterized in this mainland-Asian species. Wang, et al., found that domesticated mandarins fell into two genetic clusters that linked to different branches of the tree of wild mandarins, had different deduced population histories and had distinct patterns of pomelo introgression, suggesting that they derive from separate domestication events.[31] Wu, et al., would later extend this observation, similarly detecting two divergent subspecies within the wild populations that gave rise to Wang's northern and southern domesticate classes, which they described as 'common mandarins' and mangshanyeju (Mangshan wild mandarins).[8] It was specifically in the latter that a genetic mutation caused by the insertion of a transposable element adjacent to the CitRKD1 gene led to the ability of these mandarins to reproduce asexually through apomixis, a characteristic passed down to the subspecies' hybrid descendants such as hybrid mandarins, oranges, lemons and grapefruit.[8]

A distinct class of mandarins are native to the Japanese and neighboring islands. Initial characterization of one of these, the Tachibana orange (Tanaka's Citrus tachibana), native to Taiwan, the Ryukyu Islands and southern Japan, classified it as a subspecies nesting within the wild mandarins of the East-Asian mainland.[31][7] However, a directed study of these island cultivars revealed the existence of a second mandarin true-species that diverged from the mainland species between 2.2 and 2.8 million years ago, following the geographical isolation of the islands through rising sea levels. Unlike the mainland species, this Ryukyu mandarin, named C. ryukyuensis, reproduces sexually. The previously-characterized island cultivars, including the Tachibana, proved to be either natural F1 hybrids between this native Ryukyu mandarin and mainland mandarin species that had recolonized the islands after a period of isolation, or else later agricultural hybrids with introduced Asian cultivars.[8]

All characterized commercial varieties called mandarins are actually inter-species hybrids.[4][32] Wu, et al., divided mandarins into three types, based on their degree of hybridization. In addition to genetically pure mandarins, a second type are the result of hybridization with pomelos followed by subsequent backcrossing with mandarins to retain only a few pomelo traits. The third type arose more recently from the crossing of these hybrids again with pomelos or sweet oranges (which are themselves crosses of hybrid mandarins and pomelos). This produces mandarins with more, longer stretches of pomelo DNA.[7] Some commercial mandarins are hybrids with lemons, while several were found to have a significant contribution (35–65%) from papedas.[30]

'Mangshan wild mandarin' is a name used for all of the similar-looking wild mandarin-like fruit of the Mangshan area, but has been found to include two genetically-distinct groups, one representing pure, wild "true" mandarins (the mangshanyeju subspecies of C. reticulata), and the other the genetically-distinct and only distantly-related species, the

mangshanyegan (C. mangshanensis), akin to another local fruit known as the yuanju,[31] and found to be the most distant branch of all the citrus.[7]

In a limited genomic analysis, Feroniella was found to cluster with C. reticulata deep within Citrus,[26][28] leading botanist David Mabberley to propose that the sole member of this genus, F. lucida, be moved to the genus Citrus and rechristened C. lucida.[27][28] Though this has received a degree of acceptance, two modern phylogenetic studies obtained results in conflict with Mabberley's, and retained Feronioella as a distinct genus closely related to Luminia, with which Swingle had placed Feroniella in a grouping referred to as 'wood apples'.[33]

Pomelos

The pomelo (Citrus maxima), a second of the core species from which most citrus hybrids have derived, is native to southeast Asia. Among the hybrids deriving from mandarin/pomelo crosses, there is a direct correlation between the proportion of pomelo DNA in the hybrid and fruit size, while the more palatable mandarins are those that have received specific genes from pomelos that alter their acidity.[7] Some of the more common pomelos are genetically pure, while a number have a single small region of introgressed mandarin DNA on one chromosome, the result of a cross followed by extensive backcrossing with pomelo.[34]

Citrons

Varieties of true (non-hybrid) citron (Citrus medica) have distinctly different forms. The citron usually propagates by cleistogamy, a self-pollination within an unopened flower, and this results in the lowest levels of heterozygosity among the citrus species.[7] Because of this, it will generally serve as the male parent of any hybrid progeny. Many citron varieties were proven to be non-hybrids despite their rather dramatic morphological differences;[24][35][36][6][37][38] however, the florentine citron is probably of hybrid origin. Genetic analysis of citrons has shown that they divide into three groups. One cluster consists of wild citrons that originated in China and produce non-fingered fruit with pulp and seeds. A second cluster, also native to China, consist of the fingered citrons, most of which are seedless and must be propagated artificially. The third cluster represents the Mediterranean citrons, thought to have originally been introduced there from India.[39]

Some

Mountain citron is a complex citrus hybrid that only includes trace amounts of true citron.[30]

Papedas

Swingle coined the Citrus subgenus Papeda to separate its members from the more edible citrus that also differ from other citrus in having stamens that grow separately, not united at their base.[40] He included in this group the kaffir lime (Citrus hystrix), as well as its likely taxonomic synonym the micrantha (Citrus micrantha), Ichang papeda (Citrus cavaleriei). Since the latter two species locate to different branches of the citrus phylogenetic tree, the group would be polyphyletic and not a valid division.[41][24] Both the micrantha and the Ichang papeda have also given rise to hybrids with other citrus. Sometimes included among the papedas was the mountain citron, not affiliated with the true citrons, and subsequently found to be a pure species most closely related to kumquats.[12]

Kumquats

× Citrofortunella
.

Subsequent study of the many commercial citrus lineages revealed such complexity that the genera could not be separated,

The Flora of China unites all kumquats as the single species, Citrus japonica.[44] Based on chromosomal analysis, Yasuda, et al., identified Jiangsu and Malayan kumquats as hybrids and see the remainder of the Eufortunella subgenus as a single species, while retaining a distinct species designation for the Hong Kong kumquat.[45]

Australian and New Guinean species

Oxanthera (false orange) all cluster with the Australian limes as members of Citrus.[26][46] The outback lime is a desert lime agriculturally selected for more commercial traits, while some commercial varieties of the Australian lime are hybrids with mandarins, lemons, and/or sweet oranges. Clymenia, will hybridize with kumquats and some limes
.

Trifoliate orange

The

Poncirus, but Mabberley and Zhang reunited the genera Swingle had separated back into Citrus.[13] Early phylogenetic analysis nested Poncirus within the citrus, consistent with a single genus,[24][48][26][41] but the genomic sequencing of Wu, et al., placed it outside the cluster representing Citrus, and the authors retained a separate genus Poncirus.[7] Ollitrault, Curk and Krueger indicate that the majority of data are consistent with the enlarged Citrus that includes the trifoliate orange, though they recognize that many botanists still follow Swingle.[13] A further complication to the placement of Poncirus is the conflicting phylogenetic data: its nuclear genome places Poncirus as an outgroup to other citrus, while its chloroplast DNA (cpDNA) nests within a Citrus subclade. This led Talon, et al. to conclude that the trifoliate orange likely is either the progeny of an ancient hybridization between a core citrus and an unidentified more distant relative, or at some time in its history acquired an introgressed cpDNA genome from another species.[10]

A second trifoliate orange, Poncirus polyandra, was discovered in

China) in the 1980s.[41] Zhang and Mabberley later concluded this was likely a hybrid between the trifoliate orange and some other Citrus.[49] However, recent genomic analysis of P. polyandra showed low heterozygosity,[50] the opposite of what one would expect for a hybrid. Were Poncirus subsumed into Citrus, C. polyandra would be unavailable, so C. polytrifolia has been suggested as a replacement species name for this Yunnan trifoliate orange.[51]

Photo gallery

Hybrids

Sweet oranges; G: Grapefruits. Figure from Curk, et al. (2014).[52]

Citrus hybrids include many

hybrid names, marked with a multiplication sign after the word Citrus (or abbreviation C.); for example, the Key lime is Citrus × aurantifolia, and also are referred to by joining the names of the crossed species or hybrids that produced them, as with sunquat
– C. limon × japonica. Styling a hybrid as such a cross between two species can present challenges. In some cases the parental species that gave rise to a hybrid have yet to be determined, while genotyping reveals some hybrids to descend from three or more ancestral species. In the Ollitrault system, a hybrid will be given a species name corresponding to the ancestral species contributions to it, as well as a distinctive variety name.

Labelling of hybrids

Hybrid taxonomy is inconsistent. There is disagreement over whether to assign species names to hybrids, and even modern hybrids of known parentage are sold under general common names that give little information about their ancestry, or even imply technically incorrect identity. This can be a problem for those who cannot eat some citrus varieties. Drug interactions with chemicals found in some citrus, including grapefruit and Seville oranges,[53][54] make the ancestry of citrus fruit of interest: many commonly sold citrus varieties are grapefruit hybrids[55][56] or pomelo-descended grapefruit relatives. One medical review has advised patients on medication to avoid all citrus juice,[53] although some citrus fruits contain none of the problematic furanocoumarins.[56] Citrus allergies can also be specific to only some fruit or some parts of some fruit.[57][58][59]

Major citrus hybrids

The common oranges as well as the grapefruits are hybrids between the mandarin and the pomelo.
A variety of lumia

The most common citrus hybrids that are sometimes treated as a species by themselves, especially in folk taxonomy, are:

  • orange color of the mandarin in their outer peels and segments, and are easier to peel than the pomelos. Oranges are all intermediate between the two ancestors in size, flavor and shape.[4][60] The bitter orange and sweet orange both arose from mandarin-pomelo crosses, the former involving a pure mandarin, the latter with a mandarin already containing small amounts of pomelo.[7]
  • Grapefruit: grapefruits, like oranges, include genetic contributions from both mandarin and pomelo, but more of the latter,[61] arising from a natural backcross of a sweet orange with a pomelo.[34] The 'cocktail grapefruit', or mandelo, is distinct, instead the product of a low-acid pomelo variety hybridized with a mandarin that itself was a cross between two distinct mandarin stocks.[7]
  • Lemon: "true" lemons derive from one common hybrid ancestor, having diverged by mutation. The original lemon was a hybrid between a male citron and a female sour orange, itself a pomelo/pure-mandarin hybrid; citrons contribute half of the genome, while the other half is divided between pomelo and mandarin.[7][62] There are other hybrids also known as 'lemons'. Rough lemons arose from a cross between citron and mandarin, without the pomelo contribution found in true lemons, while the Meyer lemon comes from a citron crossed with a sweet (as opposed to sour) orange.[16]
  • Limes: A highly diverse group of hybrids go by this name. Rangpur limes, like rough lemons, arose from crosses between citron and mandarin. The sweet limes, so-called due to their low acid pulp and juice, come from crosses of citron with either sweet or sour oranges, while the Key lime arose from a cross between a citron and a micrantha.[16]

All of these hybrids have in turn been bred back with their parent stocks or with other pure or hybrid citrus to form a broad array of fruits. Naming of these is inconsistent, with some bearing a variant of the name of one of the parents or simply another citrus with superficially-similar fruit, a distinct name, or a

portmanteau of ancestral species. The Ponderosa lemon (Citrus limon × medica) and Florentine citron (Citrus × limonimedica) are both true lemon/citron hybrids, the Bergamot orange is a sweet orange/lemon hybrid and the Oroblanco is a grapefruit/pomelo mix, while tangelos are tangerine (mandarin)/pomelo or mandarin/grapefruit hybrids, orangelos result from grapefruit backcrossed with sweet orange, and a sweet orange backcrossed with a tangerine gives the tangor.[34] One lumia, a member of the sweet lemons, is the product of crossing a lemon with a pomelo/citron hybrid, though another lumia variety, the Pomme d'Adam, is a micrantha/citron cross, like the Key lime. The most common and commercially popular 'limes', the Persian limes, are Key lime/lemon hybrids that combine the genetic lineages of four ancestral citrus species: mandarin, pomelo, citron and micrantha.[16]

While most other citrus are

tetraploid.[16]

Historically, hybrids with similar characteristics have been placed together in a number of hybrid species, yet relatively recent genomic analysis has revealed some hybrids assigned to the same species to be of quite distinct ancestry. No alternative system of grouping fruit in hybrid species has been adopted.

Hybrids from other citrus species

While most citrus hybrids derive from the three core species, hybrids have also been derived from the micrantha, Ichang papeda,

Indian wild orange, once suggested as a possible ancestor of today's cultivated citrus fruits,[63] yielded conflicting phylogenetic placements in more limited genetic analysis,[24][64] but study of nuclear markers and chloroplast DNA showed it to be of maternal citron lineage, with further genetic contributions from mandarin and papeda.[30]

Citrofortunella

A large group of commercial hybrids involve the kumquat, Fortunella in the Swingle system. Citrofortunella was coined as a genus containing intergeneric hybrids between members of the Citrus and the Fortunella, and is named after its parent genera.[65] Such hybrids often combine the cold hardiness of the kumquat with some edibility properties of the other Citrus species. As members of a hybrid genus, these crosses were marked with the multiplication sign before the genus name, for example × Citrofortunella microcarpa. With the return of kumquats to within Citrus, Citrofortunella are no longer viewed as being intergeneric hybrids and thus likewise belong in Citrus, while Citrofortunella as a distinct genus name would no longer be valid.[43] Examples of the Citrofortunella include the calamansi, limequat, and yuzuquat, crossing kumquat with tangerine, Key lime, and yuzu respectively.

Citroncirus

As with kumquats, the

sweet oranges, and the citrumelo, a hybrid of trifoliate orange and 'Duncan' grapefruit
. As with Citrofortunella, were Poncirus subsumed into Citrus, these hybrids would no longer be intergeneric, and would likewise fall within Citrus, rendering Citroncirus invalid.

Graft hybrids

Bizzarria, an unusual graft-chimera.

Due to the sterility of many of the genetic hybrids as well as disease- or temperature-sensitivity of some Citrus trees, domesticated citrus cultivars are usually propagated via grafting to the rootstock of other, often hardier though less palatable citrus or close relatives. As a result, graft hybrids, also called graft-chimaeras, can occur in Citrus. After grafting, the cells from the scion and rootstock are not somatically fused, but rather the cells of the two intermix at the graft site, and can produce shoots from the same tree that bear different fruit. For example, the 'Faris' lemon, has some branches with purple immature leaves and flowers with a purple blush that give rise to sour fruit, while other branches produce genetically distinct sweet lemons coming from white flowers, with leaves that are never purple.[66] Graft hybrids can also give rise to an intermixed shoot that bears fruit with a combination of the characteristics of the two contributing species due to the presence of cells from both in that fruit. In an extreme example, on separate branches Bizzarria produces fruit identical to each of the two contributing species, but also fruit that appears to be half one species and half the other, unmixed. In taxonomy, graft hybrids are distinguished from genetic hybrids by designating the two contributing species with a plus sign between the individual names (Citrus medica + C. aurantium).

See also

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