title: Changes in Anthocyanin Production during Domestication ofCitrus.
abstract: Mandarin (Citrus reticulata), citron (Citrus medica), and pummelo (Citrus maxima) are important species of the genusCitrusand parents of the interspecific hybrids that constitute the most familiar commercial varieties ofCitrus: sweet orange, sour orange, clementine, lemon, lime, and grapefruit. Citron produces anthocyanins in its young leaves and flowers, as do species in genera closely related toCitrus, but mandarins do not, and pummelo varieties that produce anthocyanins have not been reported. We investigated the activity of theRubygene, which encodes a MYB transcription factor controlling anthocyanin biosynthesis, in different accessions of a range ofCitrusspecies and in domesticated cultivars. A white mutant of lemon lacks functional alleles ofRuby, demonstrating thatRubyplays an essential role in anthocyanin production inCitrusAlmost all the natural variation in pigmentation by anthocyanins inCitrusspecies can be explained by differences in activity of theRubygene, caused by point mutations and deletions and insertions of transposable elements. Comparison of the allelic constitution ofRubyin different species and cultivars also helps to clarify many of the taxonomic relationships in different species ofCitrus, confirms the derivation of commercial varieties during domestication, elucidates the relationships within the subgenusPapeda, and allows a new genetic classification of mandarins.
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.); eugenio.butelli@jic.ac.uk.|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.); eugenio.butelli@jic.ac.uk.|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.); eugenio.butelli@jic.ac.uk.|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.); eugenio.butelli@jic.ac.uk.|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.); eugenio.butelli@jic.ac.uk.|University of California, Riverside, California 92521 (C.R.); eugenio.butelli@jic.ac.uk.|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.); eugenio.butelli@jic.ac.uk.|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and eugenio.butelli@jic.ac.uk.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.) eugenio.butelli@jic.ac.uk.
authors.forename: Eugenio
authors.identifier: 0000-0001-6397-277X
authors.initials: E
authors.lastname: Butelli
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Andrés
authors.initials: A
authors.lastname: Garcia-Lor
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Concetta
authors.initials: C
authors.lastname: Licciardello
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Giuseppina
authors.initials: G
authors.lastname: Las Casas
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Lionel
authors.identifier: 0000-0001-9147-9130
authors.initials: L
authors.lastname: Hill
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Giuseppe Reforgiato
authors.identifier: 0000-0001-7663-2299
authors.initials: GR
authors.lastname: Recupero
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Manjunath L
authors.identifier: 0000-0002-8646-9293
authors.initials: ML
authors.lastname: Keremane
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Chandrika
authors.initials: C
authors.lastname: Ramadugu
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Robert
authors.initials: R
authors.lastname: Krueger
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Qiang
authors.identifier: 0000-0003-1786-9696
authors.initials: Q
authors.lastname: Xu
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Xiuxin
authors.identifier: 0000-0003-4490-4514
authors.initials: X
authors.lastname: Deng
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Anne-Laure
authors.initials: AL
authors.lastname: Fanciullino
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Yann
authors.initials: Y
authors.lastname: Froelicher
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Luis
authors.identifier: 0000-0001-5163-5960
authors.initials: L
authors.lastname: Navarro
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom (E.B., L.H., C.M.).|Instituto Valenciano de Investigaciones Agrarias, 46113 Moncada, Valencia, Spain (A.G.-L., L.N.).|Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per l'Agrumicoltura e le Colture Mediterranee, 95024 Acireale, Italy (C.L., G.R.-R.).|Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, 95123 Catania, Italy (G.L.C.).|United States Department of Agriculture-Agricultural Research Service National Clonal Germplasm Repository for Citrus and Dates, Riverside, California 92507-5437 (M.L.K., R.K.).|University of California, Riverside, California 92521 (C.R.).|Key Laboratory of Horticultural Plant Biology of the Ministry of Education, Huazhong Agricultural University, Wuhan 430070, People's Republic of China (Q.X., X.D.).|Institut National de la Recherche Agronomique, UR1115 PSH, F-84914 Avignon, France (A.-L.F.); and.|CIRAD, Unité Mixte de Recherche AGAP, Station Institut National de la Recherche Agronomique, F-20230 San Giuliano, France (Y.F.).
authors.forename: Cathie
authors.identifier: 0000-0002-3640-5080
authors.initials: C
authors.lastname: Martin
mesh_terms: D000483:Alleles; D000872:Anthocyanins / Q000096:biosynthesis*; D001483:Base Sequence; D002957:Citrus / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D000071278:Domestication; D035264:Flowers / Q000235:genetics / Q000378:metabolism*; D017353:Gene Deletion; D018506:Gene Expression Regulation, Plant; D005838:Genotype; D009154:Mutation; D010802:Phylogeny; D010858:Pigmentation / Q000235:genetics; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism*; D010940:Plant Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism; D018626:Retroelements / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012689:Sequence Homology, Nucleic Acid; D013045:Species Specificity; D014157:Transcription Factors / Q000145:classification / Q000235:genetics / Q000378:metabolism
chemical_list: D000872:Anthocyanins; D010940:Plant Proteins; D018626:Retroelements; D014157:Transcription Factors