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The origin of

Guohong Albert Wu, Javier Terol, Victoria Ibanez, Antonio López-García, Estela GENOMICS ILLUMINATES THE ORIGIN AND Pérez-Román, Carles Borredá, Concha Domingo, Francisco R. Tadeo, José Carbonell-Caballero, Roberto Alonso, Franck Curk, Dongliang Du, Patrick Ollitrault, DISPERSAL OF CITRUS Mikeal L. Roose , Joaquin Dopazo, Frederick G. Gmitter Jr., Daniel S. Rokhsar and Manuel Talon

Instituto Valenciano de Investigaciones Agrarias (IVIA)

Pure , admixtures and hybrids in the Genus Citrus Pure species, admixtures and hybrids in the Genus Citrus

Common name Species name Common name Species name Corsican C. medica L. Guan-xi-mi-you pummelo C. maxima [(Burm.) Merr]. Mac Veu citron C. medica L C. grandis (Swingle, Tanaka) Citrus Risso & Poit . Sha-tian-you pummelo C. maxima [(Burm.) Merr]. PURE SPECIES HYBRIDS ADMIXTURES Buddha’s hand citron C. medica L. (Noot.) Swingle C. grandis (Swingle, Tanaka) var. Sarcodactylus , C. x paradisi (Macfadyen) oranges Mandarins Humpang citron C. medica L. cv. Marsh Sun Chu Sha Kat mandarin C. reticulata (Blanco) C. reticulata var. Sweet , C. x sinensis L. (Osbeck) Pummelos limes Sweet oranges austera (Swingle) C. erythrosa (Tanaka) cv. Washington Navel Tachibana mandarins Rough limes Sour orange, C. x aurantium L. Tachibana mandarin C. tachibana (Mak.) Tan cv.Sevillano C. reticulata (Blanco) Sun Chu Sha Kat mandarins Mexican limes , cv.Eureka C. x limon L. (Burm. f.) Sunki mandarin C. sunki (Hayata, Hort. ex Tanaka Eremorages Australian desert Eremocitrus glauca (Lindl.) Swingle Australian desert limes (sour mandarin, suanju) C. reticulata (Blanco) C. * glauca (Lindl.) Burkill Calamondins Cleopatra mandarin C. reshni (Hort. ex Tanaka) Eremocitrus glauca (Lindl.) Swingle Australian finger limes C. reticulata (Blanco) Eremorange. Eremocitrus glauca x Citrus sinnensis. Australian round limes Changsha mandarin Citrus reticulata (Blanco) Australian desert lime Huanglingmiao mandarin C.* reticulata (Hort. ex Tanaka) Australian finger lime Microcitrus australasica (F.Muell.) Swingle Satsuma (unshiu) mandarin, C. * unshiu [(Mak.) Marc] C. australasica F. Muell. cv. Owari C. *reticulata (Swingle) Micranthas C. *reticulata (Blanco, Swingle) Australian finger lime Microcitrus australasica (F.Muell.) Swingle Mangshan mandarins (Chinese honey orange) C. australasica F. Muell Dancy mandarin, C. * tangerina (Tanaka) Papedas Dancy C. *reticulata (Swingle) Australian round lime Microcitrus australis Swingle Willowleaf mandarin C. deliciosa (Ten. Hort. ex Tanaka) C. australis (A. Cunn. ex Mudie) mandarin, C. x clementina (Hort. ex Tanaka) Australian round lime Microcitrus australis Swingle Poncirus cv. Clementina de Nules C.x reticulata (Swingle) C. australis (A. Cunn. ex Mudie) King mandarin C. * nobilis (Lour.) , Nagami Fortunella (Lour.) Swingle C. *reticulata (Swingle) Calamondin C. madurensis (Lour.) W. mandarin C. reticulata (Blanco) Mexican/ C. * aurantifolia (Christm.) Swingle Rangpur lime C. x limonia (Osbeck) , Biasong C. micrantha (Wester) Mangshan mandarin C. mangshanensis Red C x jambhiri (Lush) Ichang C. ichangensis (Swingle) Low pummelo C. maxima [(Burm.) Merr]. (Siamese Sweet) C. grandis (Swingle, Tanaka) Poncirus trifoliata (L.) Raf. Chinese box orange (Poir.)Tenore Chandler pummelo C. maxima [(Burm.) Merr].

Genealogy of domesticated citrus Chloroplast phylogenetic of the genus Citrus

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Nuclear phylogenetic tree of the genus Citrus Nuclear phylogenetic tree of the genus Citrus

The oldest citrus fossil specimen Chronogram of citrus speciation

Entire margin Late Miocene Pliocene Pleistocene Citrus maxima

ASIAN RADIATION

Intramarginal vein 8.0-6.0 Ma Late Miocene Citrus reticulata Citrus aurantifolia AUSTRALIAN RADIATION 4.6-4-1 Ma Early Pliocene Articulated and winged TACHIBANA SPECIATION Citrus maxima Citrus ichangensis 2,4-2.3 Ma Citrus micrantha Early Pleistocene Ma Citrus linczangensis (~ 8 Ma, midpoint of Late Miocene) Yunnan, . Sanping Xie et al.(2013)

The center of origin of citrus and its dispersal Biogeography of the genus Citrus

Biogeography of the genus Citrus

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Biogeography of the genus Citrus Biogeography of the pure Citrus species

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7 25. 7 25. 24 24 26 26 20 20 42 14 5 3130 21 145 6 39 9 9 41 372740 356 2 3629 2 18 1 18 1 23 1213 15 8 28 32 23 1213 158 10 38 44 10. 19 34 33 19 4 4 16 45 16 11 11

17 17 17

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Blue = pure species Black = hybrids Red = admixtures

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The center of origin of citrus Biogeography of the pure Citrus species

C. mangshanensis Tachibana Sun Chu Cha Kat C. linczanensis C. ichangensis Citron Pummelo Kumquat

Micrantha

Australian limes

The Asian radiation and the monsoon Radiations during Late Miocene in the foothills of the Himalaya

Late Miocene 8,0-6,4 Ma

Ma

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The Australian radiation. Land bridges between The Tachibana speciation. Land bridges between main Wallacea and Australia land and , the Ryukyu archipelago and

WEST EAST Aglaia Alocasia Begonia Pseuduvaria Neonauclea Uvaria Palm lineages Bridelia Begonia … etc

The center of origin of citrus and ancient dispersal routes Summary

2,4 Ma Genomic analysis has revealed that the genus Citrus is formed by pure species, admixtures and hybrids. Based on the analyses of the pure species, we propose that: 8-6 Ma • The center of origin of citrus was located in between the provinces of Assam and Yunnan and northern Myanmar.

• The dispersal of citrus followed a predominant west to east direction with three main radiations:

• The Asian radiation occurred in the Late Miocene and was driven by a dramatic climate change of the intensity of the Indian summer monsoon.

• The Australian radiation was enabled by the Early Pliocene 4,6 Ma orogeny that provoked the emergence of submerged land and corridors between the Wallacea and Australia

• Radiations in islands of Eastern Asian during the Early Pleistocene were due to expansion of glaciers that reduced sea levels rising land bridges between continental Asia and Japan.

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