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Link to original content: https://pubmed.ncbi.nlm.nih.gov/34312382
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. 2021 Jul 26;12(1):4377.
doi: 10.1038/s41467-021-24653-0.

Diversification of mandarin citrus by hybrid speciation and apomixis

Guohong Albert Wu #  1 , Chikatoshi Sugimoto #  2 , Hideyasu Kinjo  3 , Chika Azama  2 , Fumimasa Mitsube  3 , Manuel Talon  4 , Frederick G Gmitter Jr  5 , Daniel S Rokhsar  6   7   8   9
Affiliations

Diversification of mandarin citrus by hybrid speciation and apomixis

Guohong Albert Wu et al. Nat Commun. .

Abstract

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.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Population structure, genetic admixture, and heterozygosity of east Asian citrus.
a Multidimensional scaling (MDS) plot of 51 citrus accessions. Projection onto the first two principal coordinates (upper panel) shows C. ryukyuensis as a distinct population from tachibana, shiikuwasha, and other Ryukyuan hybrids (yukunibu and deedee). The third principal coordinate (lower panel) separates the two Mangshan wild mandarins (MS) from other mandarins. It also separates tachibana from shiikuwasha. For easier visualization, accessions with significant pummelo ancestry (pummelos, oranges, some mandarins, yukunibus) are not shown in the lower panel. See Supplementary Data 1 and 3 for accession code and names. b Four-way admixture plot of 53 citrus accessions based on local ancestry inference. PU=pummelo (C. maxima), RK=C. ryukyuensis, MS=mangshanyeju, MA=common mandarin, MM=generic C. reticulata without subspecies assignment (MS vs MA), UNK=unknown. Note that tachibana has more MS alleles than shiikuwasha and other Ryukyuan hybrids. Some wild mandarins (M01, M04) are hybrids with nearly equal contribution from the two subspecies of MS and MA. Common mandarins display varying degree of MS admixture. c Heterozygosity distribution violin plot for the same accessions as in b), for non-overlapping windows of 500,000 callable sites. C. ryukyuensis shows the lowest heterozygosity compared to tachibana, shiikuwasha and other hybrid types as well as accessions from C. reticulata and C. maxima. Median and quartiles are denoted by the white dot and black bar limits respectively, and whiskers are 1.5× inter-quartile range. Source data are provided as a Source Data file.
Fig. 2
Fig. 2. Chronogram of east Asian mandarin citrus speciation and biogeography in the Ryukyu Arc and mainland Japan.
a Population divergence times of C. ryukyuensis (2.2–2.8 Mya) and two subspecies of mainland Asian mandarins (C. reticulata): common mandarin and mangshanyeju (1.4–1.7 Mya). Extant common mandarins are recent admixtures with both mangshanyeju and pummelos. b Geological history of the Ryukyu Arc and evolutionary origins of east Asian citrus during four representative time periods: (1) initial radiation of citrus during the late Miocene with subsequent dispersal to regions including Mangshan of the Nanling mountain range. The exact arrival time of primitive mandarins at Mangshan cannot be determined and could be as late as the Pliocene epoch (5.3–2.6 Mya) (top left), (2) geographical isolation and genetic divergence of C. ryukyueneis in the Ryukyu Arc from mainland Asian mandarins during early Pleistocene (top right), (3) divergence of mangshanyeju and common mandarins (bottom left), and (4) current distribution of east Asian citrus with C. ryukyuensis ancestry in the Ryukyu Arc and mainland Japan, as a result of distinct hybridization events with different migrant mainland mandarins (bottom right). (Maps are adapted from Kimura with paleo-landmasses in light green.) Source data underlying Fig. 2a are provided as a Source Data file.
Fig. 3
Fig. 3. Hybrid speciation and admixture map of Ryukyuan and mainland Japanese citrus.
a Origin of Ryukyuan and mainland Japanese citrus types (tachibana, shiikuwasha, yukunibu) derived from four ancestral populations. Thick arrows denote ancestry involving multiple individuals from a population, whereas a thin arrow stands for single individual ancestry. Dotted and solid lines from the top row denote small and significant introgression, respectively. For example, RK3 has small amount of pummelo admixture whereas kunenbo has significant pummelo introgression. The shiikuwashas are half-sibs sharing the same mainland Asian mandarin parent (RK3) but different C. ryukyuensis parents. Kunenbo (KB3) is the seed parent of the yukunibu group. b Four-way admixture map for Ryukyuan and mainland Japanese citrus types. Population code as in Fig. 1b. Tachibana genomes are characterized by both significant admixture with MS and segments of diploid C. ryukyuensis genotype. SH4 is a seedless shiikuwasha. Source data underlying Fig. 3b are provided as a Source Data file.
Fig. 4
Fig. 4. Ancestry of apomixis alleles and two subspecies of mainland Asian mandarins (C. reticulata).
a Diversity of the apomixis alleles in mandarins and inter-specific mandarin hybrids. The ancestral allele does not have the MITE transposon insertion in the promoter of the CitRKD1 gene regulating citrus apomixis. Derived alleles with the MITE insertion are dominant for the nucellar embryony phenotype. Four MITE haplotypes in two haplogroups (H1=H1A and H1B; H2=H2A and H2B) are observed among sequenced mandarins and hybrids with each black line denoting a segregating SNP. Listed next to each MITE allele type are representative citrus accessions containing that allele. b Genetic ancestry of the citrus polyembryonic locus (200 kb region flanking CitRKD1 gene). Fifty-five accessions derived from six  progenitor species are analyzed with ADMIXTURE and the eight-population (K=8) structure is presented with additional figures shown in Supplementary Fig. 8. (PU=pummelo, CI=citron, RK=C. ryukyuensis, IC=Ichang papeda, FO=Fortunella (kumquat), MA= common mandarin, h1 and h2 have mangshanyeju ancestry). Accessions with h1 ancestry contain MITE H1A or H1B, whereas those with h2 ancestry have MITE H2A or H2B. MS1 and MS2 are two mangshanyeju accessions. All sequenced polyembryonic accessions carry the dominant allele with the MITE insertion and have mangshanyeju ancestry at this locus, whereas monoembryonic accessions have common mandarin but not mangshanyeju ancestry. c Genome-wide local ancestry inference of mainland East Asian citrus with four ancestral populations including two subspecies of C. reticulata (MS, MA). Population code as in Fig. 1b. This figure complements Fig. 3b by considering 21 accessions without C. ryukyuensis ancestry. Note that the apomixis locus is located near the end of chromosome 1 (based on the Clementine reference sequence) which exhibits extensive MS admixture in common mandarins relative to other chromosomes. MS admixture is widespread in all sequenced mandarins. Two wild mandarins (M01=Daoxian wild mandarin and clonal relatives, M04=Suanpangan) show hybrid ancestry with nearly equal contribution from MS and MA. Source data underlying Fig. 4b and c are provided as a Source Data file.
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References

    1. Swingle, W. T. & Reece, P. C. in The citrus industry, revised 2nd ed., History, World Distribution, Botany, and Varieties Vol. 1 (ed.s W. Reuther, H. J. Webber, & L. D. Batchelor) 190–430 (University of California, Berkeley, California, USA, 1967).
    1. Tanaka T. Fundamental discussion of Citrus classification. Stud. Citrologica. 1977;14:1–6.
    1. USDA Foreign Agricultural Service. Citrus: world markets and trade. https://apps.fas.usda.gov/psdonline/circulars/citrus.pdf (2021).
    1. Wang L, et al. Genome of wild mandarin and domestication history of mandarin. Mol. Plant. 2018;11:1024–1037. doi: 10.1016/j.molp.2018.06.001. - DOI - PubMed
    1. Tanaka T. A revision of Ryukyu Rutaceae-Aurantioideae, Revisio Aurantiacearum X. Sci bull Agr Home Eco Division. Univ. Ryukyus. 1957;4:91–116.

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