Diversification of mandarin citrus by hybrid speciation and apomixis

Wu, Guohong Albert; Sugimoto, Chikatoshi; Kinjo, Hideyasu; Azama, Chika; Mitsube, Fumimasa; Talon, Manuel; Gmitter, Jr., Frederick G.; Rokhsar, Daniel S.

doi:10.1038/s41467-021-24653-0

Diversification of mandarin citrus by hybrid speciation and apomixis

Journal Article · Mon Jul 26 00:00:00 EDT 2021 · Nature Communications

DOI:https://doi.org/10.1038/s41467-021-24653-0· OSTI ID:1820335

^[1]; Sugimoto, Chikatoshi ^[2]; Kinjo, Hideyasu ^[3]; ^[2]; Mitsube, Fumimasa ^[3]; Talon, Manuel ^[4]; ^[5]; ^[6]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Okinawa Inst. of Science and Technology Graduate Univ. (Japan)
Okinawa Prefectural Agricultural Research Center (Japan)
Inst. Valenciano de Investigaciones Agrarias (Spain)
Univ. of Florida, Lake Alfred, FL (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Okinawa Institute of Science and Technology Graduate Univ. (Japan); Univ. of California, Berkeley, CA (United States)

The origin and dispersal of cultivated and wild mandarin and related citrus are poorly understood. Here, comparative genome analysis of 69 new east Asian genomes and other mainland Asian citrus reveals a previously unrecognized wild sexual species native to the Ryukyu Islands: C. ryukyuensis sp. nov. The taxonomic complexity of east Asian mandarins then collapses to a satisfying simplicity, accounting for tachibana, shiikuwasha, and other traditional Ryukyuan mandarin types as homoploid hybrid species formed by combining C. ryukyuensis with various mainland mandarins. These hybrid species reproduce clonally by apomictic seed, a trait shared with oranges, grapefruits, lemons and many cultivated mandarins. We trace the origin of apomixis alleles in citrus to mangshanyeju wild mandarins, which played a central role in citrus domestication via adaptive wild introgression. Our results provide a coherent biogeographic framework for understanding the diversity and domestication of mandarin-type citrus through speciation, admixture, and rapid diffusion of apomictic reproduction.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1820335

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (55)

Dispersal ecology of the maritime plants in the Ryukyu Islands, Japan Nakanishi, Hiroki Ecological Research, Vol. 3, Issue 2 https://doi.org/10.1007/BF02346937	journal	August 1988
Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications Ota, Hidetoshi Researches on Population Ecology, Vol. 40, Issue 2 https://doi.org/10.1007/BF02763404	journal	October 1998
Phylogeny and biogeography of the Viola iwagawae-tashiroi species complex (Violaceae, section Plagiostigma) endemic to the Ryukyu Archipelago, Japan Nakamura, Koh; Denda, Tetsuo; Kokubugata, Goro Plant Systematics and Evolution, Vol. 301, Issue 1 https://doi.org/10.1007/s00606-014-1076-y	journal	June 2014
Diversity of Citrus depressa Hayata (Shiikuwasha) revealed by DNA analysis Yamamoto, Masashi; Takakura, Akiko; Tanabe, Aika Genetic Resources and Crop Evolution, Vol. 64, Issue 4 https://doi.org/10.1007/s10722-016-0403-2	journal	April 2016
Distribution and evolution of citrus with S 4 and/or S 5 gene alleles for self-incompatibility with special focus on the origin of satsuma mandarin (Citrus unshiu Marc.; S f S 4 ) Zhou, Xiao-Hui; Kim, Jung-Hee; Wakana, Akira Genetic Resources and Crop Evolution, Vol. 65, Issue 3 https://doi.org/10.1007/s10722-017-0592-3	journal	December 2017
Molecular discrimination of landraces of Citrus species in the Okinawa, Japan Lam, Dinh Thi; Ishikawa, Ryuji Genetic Resources and Crop Evolution, Vol. 66, Issue 2 https://doi.org/10.1007/s10722-018-0710-x	journal	November 2018
Genetic diversity and population structure analysis of mandarin germplasm by nuclear, chloroplastic and mitochondrial markers Garcia-Lor, Andres; Luro, François; Ollitrault, Patrick Tree Genetics & Genomes, Vol. 11, Issue 6 https://doi.org/10.1007/s11295-015-0951-1	journal	November 2015
QTL mapping of mandarin (Citrus reticulata) fruit characters using high-throughput SNP markers Yu, Yuan; Chen, Chunxian; Gmitter, Frederick G. Tree Genetics & Genomes, Vol. 12, Issue 4 https://doi.org/10.1007/s11295-016-1034-7	journal	July 2016
Noemi Controls Production of Flavonoid Pigments and Fruit Acidity and Illustrates the Domestication Routes of Modern Citrus Varieties Butelli, Eugenio; Licciardello, Concetta; Ramadugu, Chandrika Current Biology, Vol. 29, Issue 1 https://doi.org/10.1016/j.cub.2018.11.040	journal	January 2019
Domestication: Colour and Flavour Joined by a Shared Transcription Factor Allan, Andrew C. Current Biology, Vol. 29, Issue 2 https://doi.org/10.1016/j.cub.2018.12.005	journal	January 2019
Genome of Wild Mandarin and Domestication History of Mandarin Wang, Lun; He, Fa; Huang, Yue Molecular Plant, Vol. 11, Issue 8 https://doi.org/10.1016/j.molp.2018.06.001	journal	August 2018
Natural Variation in CCD4 Promoter Underpins Species-Specific Evolution of Red Coloration in Citrus Peel Zheng, Xiongjie; Zhu, Kaijie; Sun, Quan Molecular Plant, Vol. 12, Issue 9 https://doi.org/10.1016/j.molp.2019.04.014	journal	September 2019
Genomics of the origin and evolution of Citrus Wu, Guohong Albert; Terol, Javier; Ibanez, Victoria Nature, Vol. 554, Issue 7692 https://doi.org/10.1038/nature25447	journal	February 2018
Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication Wu, G. Albert; Prochnik, Simon; Jenkins, Jerry Nature Biotechnology, Vol. 32, Issue 7 https://doi.org/10.1038/nbt.2906	journal	June 2014
Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction Wang, Xia; Xu, Yuantao; Zhang, Siqi Nature Genetics, Vol. 49, Issue 5 https://doi.org/10.1038/ng.3839	journal	April 2017
Hyperacidification of Citrus fruits by a vacuolar proton-pumping P-ATPase complex Strazzer, Pamela; Spelt, Cornelis E.; Li, Shuangjiang Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08516-3	journal	February 2019
Subfunctionalization of the Ruby2–Ruby1 gene cluster during the domestication of citrus Huang, Ding; Wang, Xia; Tang, Zhouzhou Nature Plants, Vol. 4, Issue 11 https://doi.org/10.1038/s41477-018-0287-6	journal	October 2018
Evolution of self-compatibility by a mutant Sm-RNase in citrus Liang, Mei; Cao, Zonghong; Zhu, Andan Nature Plants, Vol. 6, Issue 2 https://doi.org/10.1038/s41477-020-0597-3	journal	February 2020
Testing the Genetic Relation Between Two Individuals Using a Panel of Frequency-unknown Single Nucleotide Polymorphisms Lee, W. -C. Annals of Human Genetics, Vol. 67, Issue 6 https://doi.org/10.1046/j.1529-8817.2003.00063.x	journal	November 2003
Citrus linczangensis sp. n., a Leaf Fossil of Rutaceae from the Late Miocene of Yunnan, China Xie, Sanping; Manchester, Steven R.; Liu, Kenan International Journal of Plant Sciences, Vol. 174, Issue 8 https://doi.org/10.1086/671796	journal	October 2013
Phylogenetic origin of limes and lemons revealed by cytoplasmic and nuclear markers Curk, Franck; Ollitrault, Frédérique; Garcia-Lor, Andres Annals of Botany, Vol. 117, Issue 4 https://doi.org/10.1093/aob/mcw005	journal	March 2016
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
From mainland to islands: colonization history in the tree frog Kurixalus (Anura: Rhacophoridae) Yu, Guo-Hua; Du, Li-Na; Wang, Ji-Shan Current Zoology, Vol. 66, Issue 6 https://doi.org/10.1093/cz/zoaa023	journal	May 2020
The Ecological Genetics of Homoploid Hybrid Speciation Gross, B. L.; Rieseberg, L. H. Journal of Heredity, Vol. 96, Issue 3 https://doi.org/10.1093/jhered/esi026	journal	December 2004
Citrus Fruits of Japan Tanaka, TyÔZaburÔ Journal of Heredity, Vol. 13, Issue 6 https://doi.org/10.1093/oxfordjournals.jhered.a102216	journal	June 1922
Fast model-based estimation of ancestry in unrelated individuals Alexander, D. H.; Novembre, J.; Lange, K. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.094052.109	journal	July 2009
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Changes in Anthocyanin Production during Domestication of Citrus Butelli, Eugenio; Garcia-Lor, Andrés; Licciardello, Concetta Plant Physiology, Vol. 173, Issue 4 https://doi.org/10.1104/pp.16.01701	journal	February 2017
Retrotransposons Control Fruit-Specific, Cold-Dependent Accumulation of Anthocyanins in Blood Oranges Butelli, Eugenio; Licciardello, Concetta; Zhang, Yang The Plant Cell, Vol. 24, Issue 3 https://doi.org/10.1105/tpc.111.095232	journal	March 2012
Phylogeography of Ophiorrhiza japonica (Rubiaceae) in continental islands, the Ryukyu Archipelago, Japan Nakamura, Koh; Denda, Tetsuo; Kokubugata, Goro Journal of Biogeography, Vol. 37, Issue 10 https://doi.org/10.1111/j.1365-2699.2010.02342.x	journal	July 2010
Riding the Kuroshio Current: Stepping stone dispersal of the Okinawa tree lizard across the East Asian Island Arc Yang, Shang‐Fang; Komaki, Shohei; Brown, Rafe M. Journal of Biogeography, Vol. 45, Issue 1 https://doi.org/10.1111/jbi.13111	journal	October 2017
The extent of adaptive wild introgression in crops Janzen, Garrett M.; Wang, Li; Hufford, Matthew B. New Phytologist, Vol. 221, Issue 3 https://doi.org/10.1111/nph.15457	journal	October 2018
A chromosome‐scale reference genome of trifoliate orange ( Poncirus trifoliata ) provides insights into disease resistance, cold tolerance and genome evolution in Citrus Peng, Ze; Bredeson, Jessen V.; Wu, Guohong A. The Plant Journal, Vol. 104, Issue 5 https://doi.org/10.1111/tpj.14993	journal	October 2020
The Role of Hybridization in Plant Speciation Soltis, Pamela S.; Soltis, Douglas E. Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.092039	journal	June 2009
Identification of QTLs controlling aroma volatiles using a ‘Fortune’ x ‘Murcott’ (Citrus reticulata) population Yu, Yuan; Bai, Jinhe; Chen, Chunxian BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4043-5	journal	August 2017
MITE insertion-dependent expression of CitRKD1 with a RWP-RK domain regulates somatic embryogenesis in citrus nucellar tissues Shimada, Takehiko; Endo, Tomoko; Fujii, Hiroshi BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1369-3	journal	August 2018
Investigation of floristic similarities between Taiwan and terrestrial ecoregions in Asia using GBIF data Liao, Chi-Cheng; Chen, Chih-Hui Botanical Studies, Vol. 58, Issue 1 https://doi.org/10.1186/s40529-017-0171-0	journal	March 2017
Multi-lineages of Shiikuwasha (Citrus depressa Hayata) evaluated by using whole chloroplast genome sequences and its bio-diversity in Okinawa, Japan Ishikawa, Ryuji; Badenoch, Nathan; Miyagi, Kunimasa Breeding Science, Vol. 66, Issue 4 https://doi.org/10.1270/jsbbs.15151	journal	January 2016
Hybrid Origins of Citrus Varieties Inferred from DNA Marker Analysis of Nuclear and Organelle Genomes Shimizu, Tokurou; Kitajima, Akira; Nonaka, Keisuke PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0166969	journal	November 2016
Inferring the Joint Demographic History of Multiple Populations: Beyond the Diffusion Approximation Jouganous, Julien; Long, Will; Ragsdale, Aaron P. Genetics, Vol. 206, Issue 3 https://doi.org/10.1534/genetics.117.200493	journal	May 2017
A model for the domestication and diversification processes of modern citrus cultivars in Japan Shimizu, T.; Kitajima, A.; Nonaka, K. Acta Horticulturae, Issue 1230 https://doi.org/10.17660/ActaHortic.2019.1230.2	journal	January 2019
Phylogeography of plants in Taiwan and the Ryukyu Archipelago Chiang, Tzen-Yuh; Schaal, Barbara A. TAXON, Vol. 55, Issue 1 https://doi.org/10.2307/25065526	journal	February 2006
Biogeography and origin of Lilium longiflorum and L. formosanum (Liliaceae) endemic to the Ryukyu Archipelago and Taiwan as determined by allozyme diversity Hiramatsu, Michikazu; Ii, Kaori; Okubo, Hiroshi American Journal of Botany, Vol. 88, Issue 7 https://doi.org/10.2307/3558334	journal	July 2001
Polymethoxylated Flavone Content of Major Cultivars and Local Accessions of Citrus Cultivated in Kagoshima, Japan Yamamoto, Masashi; Nishiguchi, Natsuki; Shimada, Atsushi The Horticulture Journal, Vol. 88, Issue 3 https://doi.org/10.2503/hortj.UTD-050	journal	January 2019
Local Citrus Genetic Resources and Their Polymethoxyflavones Content in Northern Part of Okinawa Island [沖縄本島北部のカンキツ遺伝資源およびそのポリメトキシフラボン含量] Inafuku-Teramoto, Sayuri; Yamamoto, Masashi; Kinjyo, Hideyasu Horticultural Research (Japan), Vol. 9, Issue 3 https://doi.org/10.2503/hrj.9.263	journal	January 2010
A Survey and Isozyme Analysis of Wild Mandarin, Tachibana (Citrus tachibana (Mak.) Tanaka) Growing in Japan [日本におけるタチバナ (Citrus tachibana (Mak.) Tanaka) の分布とアイソザイム分析] Hirai, Masashi; Mitsue, Shuichi; Kita, Keiji Journal of the Japanese Society for Horticultural Science, Vol. 59, Issue 1 https://doi.org/10.2503/jjshs.59.1	journal	January 1990
Diversity of Chloroplast DNA in Various Mandarins (Citrus spp.) and Other Citrus Demonstrated by CAPS Analysis Yamamoto, Masashi; Tsuchimochi, Yui; Ninomiya, Takanori Journal of the Japanese Society for Horticultural Science, Vol. 82, Issue 2 https://doi.org/10.2503/jjshs1.82.106	journal	January 2013
Adaptive Introgression: An Untapped Evolutionary Mechanism for Crop Adaptation Burgarella, Concetta; Barnaud, Adeline; Kane, Ndjido Ardo Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00004	journal	February 2019
Pleistocene Vertebrate Faunas in the Ryukyu Islands: Their Migration and Extinction [琉球列島における更新世脊椎動物相:その渡来と絶滅] Otsuka, Hiroyuki; Takahashi, Akio Tropics, Vol. 10, Issue 1 https://doi.org/10.3759/tropics.10.25	journal	January 2000
Paleogeography of the Ryukyu Islands. Kimura, Masaaki Tropics, Vol. 10, Issue 1 https://doi.org/10.3759/tropics.10.5	journal	January 2000
Numerical Studies on Circulations and their Variations in the Western Tropical Pacific and the Propical Indian Oceans. Masumoto, Yukio Oceanography in Japan, Vol. 9, Issue 1 https://doi.org/10.5928/kaiyou.9.15	journal	January 2000
Investigation of floristic similarities between Taiwan and terrestrial ecoregions in Asia using GBIF data Liao, Chi-Cheng; Chen, Chih-Hui Figshare https://doi.org/10.6084/m9.figshare.c.3727549	collection	January 2017
MITE insertion-dependent expression of CitRKD1 with a RWP-RK domain regulates somatic embryogenesis in citrus nucellar tissues Shimada, Takehiko; Endo, Tomoko; Fujii, Hiroshi Figshare https://doi.org/10.6084/m9.figshare.c.4197446	collection	January 2018

Similar Records

Complex history of admixture during citrus domestication revealed by genome analysis

Journal Article · Mon Jun 30 00:00:00 EDT 2014 · Nature Biotechnology · OSTI ID:1241220

Genomics of the origin and evolution of Citrus

Journal Article · Wed Jan 31 19:00:00 EST 2018 · Nature (London) · OSTI ID:1543733

Cytogenetics and reproductive behavior of 48-chromosome pearl millet x Pennisetum squamulatum derivatives

Journal Article · · Crop Science; (USA) · OSTI ID:5852640

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Agricultural genetics
Evolutionary genetics
Genetic variation
Plant domestication

Diversification of mandarin citrus by hybrid speciation and apomixis

Citation Formats

References (55)

Similar Records

Related Subjects