Citrus trifoliata

Life-forms

Classification System: APG IV

Superregnum: Eukaryota
Regnum: Plantae
Cladus: Angiosperms
Cladus: Eudicots
Cladus: Core eudicots
Cladus: Rosids
Cladus: Eurosids II
Ordo: Sapindales

Familia: Rutaceae
Subfamilia: Aurantioideae
Tribus: Aurantieae
Subtribus: Citrinae
Genus: Citrus
Species: Citrus trifoliata
Name

Citrus trifoliata L. (1763)
Synonyms

Homotypic
Bilacus trifoliata (L.) Kuntze, Revis. Gen. Pl. 1: 99. 1891.
Poncirus trifoliata (L.) Raf., Sylva Tellur. 143. 1838.
Pseudaegle trifoliata (L.) Makino, Bot. Mag. (Tokyo) 16: 15. 1902.

Heterotypic
Aegle sepiaria DC., Prodr. 1: 538. 1824.
Citrus trifolia Thunb., Fl. Jap. 294. 1784.
Citrus trifoliata subf. monstrosa (T.Itô) M.Hiroe, Forest Pl. Hist. Jap. Islands 1: 209. 1974.
Citrus trifoliata var. monstrosa T.Itô, Encycl. Jap. 2: 1056. 1909.
Citrus triptera Desf., Tabl. École Bot. ed. 3: 406. 1829.
Poncirus trifoliata var. monstrosa (T.Itô) Swingle in L.H.Bailey, Stand. Cycl. Hort. 5: 2952. 1916.
Pseudaegle sepiaria (DC.) Miq., Ann. Mus. Bot. Lugduno-Batavi 2: 83. 1865.

References

Linnaeus, C. 1763: Sp. Pl., ed. 2, 1101.
The Plant List 2013. Version 1.1 Royal Botanic Gardens, Kew and Missouri Botanical Garden. Published online. Accessed: 2014 Apr 08.

Vernacular names
Deutsch: Dreiblättrige Orange
English: Trifoliate orange
français: Citronnier épineux
日本語: カラタチ
Nederlands: wilde citroen
slovenščina: Trilistnati citronovec

The trifoliate orange, Citrus trifoliata or Poncirus trifoliata, is a member of the family Rutaceae. Whether the trifoliate oranges should be considered to belong to their own genus, Poncirus, or be included in the genus Citrus is debated. The species is unusual among citrus for having deciduous, compound leaves and pubescent (downy) fruit.[2][3]

It is native to northern China and Korea, and is also known as the Japanese bitter-orange,[4] hardy orange[5] or Chinese bitter orange.

The plant is a fairly cold-hardy citrus (USDA zone 6) and will tolerate moderate frost and snow, making a large shrub or small tree 4–8 m (13–26 ft) tall. Because of its relative hardiness, citrus grafted onto Citrus trifoliata are usually hardier than when grown on their own roots.[6]

Description

The trifoliate orange is recognizable by the large 3–5 cm (1.2–2.0 in) thorns on the shoots, and its deciduous leaves with three (or rarely, five) leaflets, typically with the middle leaflet 3–5 cm (1.2–2.0 in) long, and the two side leaflets 2–3 cm (0.79–1.18 in) long. The flowers are white, with pink stamens, 3–5 cm (1.2–2.0 in) in diameter, larger than those of true citrus but otherwise closely resembling them, except that the scent is much less pronounced than with true citrus. As with true citrus, the leaves give off a spicy smell when crushed.

The fruits are green, ripening to yellow, and 3–4 cm (1.2–1.6 in) in diameter similar in size to a lime and resembling a small orange, but with a finely downy surface and having a fuzzy texture similar to a peach. The fruits also have distinctive smell from other citrus varieties and often contain a high concentration of seeds.

Uses
Cultivation

The cultivar 'Flying Dragon' is dwarfed in size and has highly twisted, contorted stems. It makes an excellent barrier hedge due to its density and strong curved thorns. Such hedges have been grown for over 50 years at Oklahoma State University in Stillwater, and are highly student-proof.[7] The plant is also highly deer-resistant.[8] In central London, mature specimens of the trifoliate orange can be seen in the gardens of St Paul's Cathedral.

Trifoliate orange and various hybrids of this plant are widely used as citrus rootstock.

Recent studies have revealed that the trifoliate orange contains auraptene at a high concentration, which is one of the functional components having immunity against citrus tristeza virus (CTV).[9]
As food

The fruits are very bitter, due in part to their poncirin content. Most people consider them inedible fresh, but they can be made into marmalade.[8] When dried and powdered, they can be used as a condiment.
Medicine
Traditional medicine

The fruits of the trifoliate orange are widely used in medical traditions of East Asia as a treatment for allergic inflammation.[10]
Taxonomy

The trifoliate orange was historically considered a member of the genus Citrus until Walter Swingle moved it to its own novel genus, Poncirus, based on its deciduous trifoliate leaves differing from other Citrus, as part of a larger reclassification that split the historical Citrus into seven genera. However, Mabberley and Zhang reunited all of Swingle's novel genera back into Citrus.[11] Early phylogenetic analysis of trifoliate orange plastids nested Poncirus within the citrus, consistent with a single genus,[12][13][14][15] but the sequencing of the nuclear genome by Wu, et al. showed its genome to be most divergent, different enough to justify retention of Poncirus as a separate genus.[16] To explain the conflict between the plastid and nuclear genomic analysis, it was speculated that the trifoliate orange is likely either the progeny of an ancient hybridization between a core citrus and an unidentified more distant relative, or at some time in its history it acquired an introgressed cpDNA genome from another species.[17] 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.[11]

A second species of trifoliate orange native to Yunnan (China) has been reported and named Poncirus polyandra.[18] Were Poncirus to be subsumed into Citrus, where C. polyandra is unavailable, the name Citrus polytrifolia has been suggested.[19] Zhang and Mabberley concluded this Yunnan cultivar is likely a hybrid between the trifoliate orange and another Citrus,[2] but recent genomic analysis of P. polyandra showed low levels of heterozygosity,[20] the opposite of what one would expect for a hybrid. This analysis dated its divergence from P. trifoliata about 2.82 million years ago.[20]

The trifoliate orange does not naturally interbreed with core Citrus taxa due to different flowering times,[21] but hybrids have been produced artificially between the trifoliate orange and other citrus. In the Swingle system, where the trifoliate orange is placed in Poncirus, a hybrid genus name has been coined for these intra-generic crosses, "× Citroncirus". The most notable of these are the citrange, a cross between the trifoliate and sweet oranges, and the citrumelo, a hybrid of trifoliate orange and 'Duncan' grapefruit. Placing the trifoliate orange in Citrus would mean these hybrids would no longer be intergeneric, but instead hybrids within Citrus. Genomic analysis of a number of these hybrids showed them all to derive from P. trifoliata and not P. polyandra.[20]
References

The Plant List: A Working List of All Plant Species, retrieved 26 March 2016
Dianxiang Zhang & David J. Mabberley, "Citrus Linnaeus, Sp. Pl. 2: 782. 1753", Flora of China online, vol. 11
Dianxiang Zhang & David J. Mabberley, "Citrus trifoliata Linnaeus, Sp. Pl., ed. 2. 2: 1101. 1763", Flora of China online, vol. 11
BSBI List 2007 (xls). Botanical Society of Britain and Ireland. Archived from the original (xls) on 2015-06-26. Retrieved 2014-10-17.
USDA, NRCS (n.d.). "Poncirus trifoliata". The PLANTS Database (plants.usda.gov). Greensboro, North Carolina: National Plant Data Team. Retrieved 31 January 2016.
"Notice to Fruit Growers and Nurseymen Related to the Naming and Release of the US-942 Citrus Rootstock" (PDF). Agricultural Research Service, USDA. 22 October 2010. pp. 1–2. Retrieved 23 October 2017.
Gerald Klingaman. "Plant of the Week. Hardy Orange or Trifoliate Orange. Latin: Poncirus trifoliat". University of Arkansas. Division of Agriculture.
Green Deane Hardy (December 2012). "Hardy Orange".
Ohta, Satoshi; Endo, Tomoko; Shimada, Takehiko; Fujii, Hiroshi (2011). "Karatachi no kankitsu torisuteza wīrusu teikōsei to rensa suru DNA mākā" [PCR Primers for Marker Assisted Backcrossing to Introduce a CTV Resistance Gene from Poncirus trifoliata (L.) Raf. into Citrus]. Shimizu, Tokuro; Kuniga, Takeshi; Yoshioka, Terutaka; Nesumi, Hirohisa; Yoshida, Toshio; Omura, Mitsuo (University of Shizuoka). Japanese Society for Horticultural Science. pp. 295–307. Retrieved 23 October 2017.
Zhou H.Y.; Shin E.M.; Guo L.Y.; Zou L.B.; Xu G.H.; Lee S.-H.; Ze K.R.; Kim E.-K.; Kang S.S.; Kim Y.S. (2007), "Anti-inflammatory activity of 21(alpha, beta)-methylmelianodiols, novel compounds from Poncirus trifoliata Rafinesque", European Journal of Pharmacology, 572 (2–3): 239–248, doi:10.1016/j.ejphar.2007.07.005, PMID 17662711
Ollitrault, Patrick; Curk, Franck; Krueger, Robert (2020). "Citrus taxonomy". In Talon, Manuel; Caruso, Marco; Gmitter, Frederick G., Jr. (eds.). The Citrus Genus. Elsevier. pp. 57–81. doi:10.1016/B978-0-12-812163-4.00004-8. ISBN 9780128121634. S2CID 242819146.
Nicolosi, E.; Deng, Z. N.; Gentile, A.; La Malfa, S.; Continella, G.; Tribulato, E. (2000). "Citrus phylogeny and genetic origin of important species as investigated by molecular markers". Theoretical and Applied Genetics. 100 (8): 1155–1166. doi:10.1007/s001220051419. S2CID 24057066.
de Araújo, Edson Freitas; Queiroza, Luciano Paganuccide; Machado, Marcos Antônio (2003). "What is Citrus? Taxonomic implications from a study of cp-DNA evolution in the tribe Citreae (Rutaceae subfamily Aurantioideae)". Organisms Diversity & Evolution. 1: 55–62. doi:10.1078/1439-6092-00058.
Bayer, Randall J.; Mabberly, David J.; Morton, Cynthia; Miller, Cathy H.; Sharma, Ish K.; Pfiel, Bernard E.; Rich, Sarah; Hitchcock, Roberta; Sykes, Steve (2009). "A molecular phylogeny of the orange subfamily (Rutaceae: Aurantioideae) using nine cpDNA sequences". American Journal of Botany. 96 (3): 668–685. doi:10.3732/ajb.0800341. PMID 21628223. S2CID 29306927.
Garcia-Lor, Andres; Curk, Franck; Snoussi-Trifa, Hager; Morillon, Raphael; Ancillo, Gema; Luro, François; Navarro, Luis; Ollitrault, Patrick (2011). "A nuclear phylogenetic analysis: SNPs, indels and SSRs deliver new insights into the relationships in the 'true citrus fruit trees' group (Citrinae, Rutaceae) and the origin of cultivated species". Annals of Botany. 111 (1): 1–19. doi:10.1093/aob/mcs227. PMC 3523644. PMID 23104641.
Wu, Guohong Albert; Terol, Javier; Ibanez, Victoria; López-García, Antonio; Pérez-Román, Estela; Borredá, Carles; Domingo, Concha; Tadeo, Francisco R; Carbonell-Caballero, Jose; Alonso, Roberto; Curk, Franck; Du, Dongliang; Ollitrault, Patrick; Roose, Mikeal L.; Dopazo, Joaquin; Gmitter, Frederick G., Jr.; Rokhsar, Daniel; Talon, Manuel (2018). "Genomics of the origin and evolution of Citrus". Nature. 554 (7692): 311–316. Bibcode:2018Natur.554..311W. doi:10.1038/nature25447. PMID 29414943. and Supplement
Talon, Manuel; Wu, Guohong Albert; Gmitter, Frederick G.; Rokhsar, Daniel S (2020). "The origin of citrus". In Talon, Manuel; Caruso, Marco; Gmitter, Frederick G., Jr. (eds.). The Citrus Genus. Elsevier. pp. 9–31. doi:10.1016/C2016-0-02375-6. ISBN 9780128121634. S2CID 87258420.
Garcia-Lor, Andres; Curk, Franck; Snoussi-Trifa, Hager; Morillon, Raphael; Ancillo, Gema; Luro, François; Navarro, Luis; Ollitrault, Patrick (2011). "A nuclear phylogenetic analysis: SNPs, indels and SSRs deliver new insights into the relationships in the 'true citrus fruit trees' group (Citrinae, Rutaceae) and the origin of cultivated species". Annals of Botany. 111 (1): 1–19. doi:10.1093/aob/mcs227. PMC 3523644. PMID 23104641.
"Citrus polytrifolia". NCBI Taxonomy Browser. Retrieved 2 February 2021.
Peng, Ze; Bredeson, Jessen V.; Wu, Guohong A.; Shu, Shengqiang; Rawat, Nidhi; Du, Dongliang; Parajuli, Saroj; Yu, Qibin; You, Qian; Rokhsar, Daniel S.; Gmitter, Frederick G. Jr; Deng, Zhanao (2020). "A chromosome‐scale reference genome of trifoliate orange (Poncirus trifoliata) provides insights into disease resistance, cold tolerance and genome evolution in Citrus". The Plant Journal. 104 (5): 1215–1232. doi:10.1111/tpj.14993. PMC 7756384. PMID 32985030.
Froelicher, Yann; Mouhaya, Wafa; Bassene, Jean-Baptiste; Costantino, Gilles; Kamiri, Mourad; Luro, Francois; Morillo, Raphael; Ollitrault, Patrick (2011). "New universal mitochondrial PCR markers reveal new information on maternal citrus phylogeny". Tree Genetics & Genomes. 7: 49–61. doi:10.1007/s11295-010-0314-x. S2CID 32371305.