Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2014 Jul;32(7):656-62.
doi: 10.1038/nbt.2906. Epub 2014 Jun 8.

Sequencing of Diverse Mandarin, Pummelo and Orange Genomes Reveals Complex History of Admixture During Citrus Domestication

Affiliations
Free PMC article

Sequencing of Diverse Mandarin, Pummelo and Orange Genomes Reveals Complex History of Admixture During Citrus Domestication

G Albert Wu et al. Nat Biotechnol. .
Free PMC article

Abstract

Cultivated citrus are selections from, or hybrids of, wild progenitor species whose identities and contributions to citrus domestication remain controversial. Here we sequence and compare citrus genomes--a high-quality reference haploid clementine genome and mandarin, pummelo, sweet-orange and sour-orange genomes--and show that cultivated types derive from two progenitor species. Although cultivated pummelos represent selections from one progenitor species, Citrus maxima, cultivated mandarins are introgressions of C. maxima into the ancestral mandarin species Citrus reticulata. The most widely cultivated citrus, sweet orange, is the offspring of previously admixed individuals, but sour orange is an F1 hybrid of pure C. maxima and C. reticulata parents, thus implying that wild mandarins were part of the early breeding germplasm. A Chinese wild 'mandarin' diverges substantially from C. reticulata, thus suggesting the possibility of other unrecognized wild citrus species. Understanding citrus phylogeny through genome analysis clarifies taxonomic relationships and facilitates sequence-directed genetic improvement.

Figures

Figure 1
Figure 1
A selection of mandarin, pummelo and orange fruits, including cultivars sequenced in this study. Pummelos (numbered 1, 2 in outline, on left) are large trees that produce very large fruit, with white, pink or red flesh color (2) and yellow or pink rinds. Most cultivars have large leaves having petioles with prominent wings. Apomictic reproduction is absent and most selections are self-incompatible. Mandarins (3–7) are smaller trees bearing smaller fruit, with orange flesh (9, 11) and rind color. Mandarins have both apomictic and zygotic reproduction and some are self-compatible. Oranges (8, 10) are generally intermediate in tree and fruit size, flesh (10) and rind color is commonly orange, and apomictic reproduction is always present. (The sour orange shown (12) is immature.)
Figure 2
Figure 2
Nucleotide diversity distribution in citrus.(a) Nucleotide heterozygosity distribution computed in overlapping 100kb windows (with 5 kb step size) across the Low acid (LAP) and Chandler (CHP) pummelo genomes and between the non-shared haplotypes of this parent-child pair (LAP/CHP) is shown. The peak at ~6 heterozygous sites/kb in all three pairwise comparisons represents the characteristic nucleotide diversity of the species C. maxima; the peak near ~1 heterozygous site/kb reflects a bottleneck in the ancestral C. maxima population after divergence from C. reticulata (Supplementary Note 10). (b) Nucleotide heterozygosity for the traditional Willowleaf mandarin (WLM) plotted along chromosome 6, computed in overlapping windows of 200 kb (with 100 kb step size). This chromosome shows an example of the clear discontinuity in single nucleotide variant heterozygosity levels between ~5/kb in the M/M segment (orange bar) and ~17/kb in the M/P segment (blue bar). (c) Nucleotide heterozygosity distribution computed in overlapping 500kb windows (with 5 kb step size) in Ponkan (PKM, solid line) and Willowleaf (WLM, dashed line) mandarins. Genomic segments are designated M/M, M/P or P/P based on a set of 1,537,264 SNPs that differentiate C. reticulata (M) from C. maxima (P). Both mandarins contain admixed segments from C. maxima introgression (M/P) as well as M/M segments, and these are plotted and normalized separately for easy comparison.. (d) Nucleotide heterozygosity distribution computed in overlapping windows of 500kb (5 kb offsets) for sweet orange (SWO) and sour orange (SSO). The three different genotypes of the SWO genome (M/M, P/P and M/P), and the SSO genotype M/P are normalized and plotted separately
Figure 3
Figure 3
Admixture patterns and nucleotide diversity in cultivated citrus. For each of the three groups of sequenced citrus, variation in nucleotide diversity (averaged over 500kb windows with step size 250kb) is shown across the genome for one representative cultivar above genotype maps (horizontal bars: green = C. maxima/C. maxima; blue = C. maxima/C. reticulata; orange= C. reticulata/C. reticulata; grey=unknown; the 9 chromosomes are numbered at the top). (a) Sweet orange (SWO) nucleotide diversity with genotype maps for SWO and sour orange (SSO). Note the C. maxima/C. maxima genotype (green segments present on chromosomes 2 and 8) in SWO. (b) Willowleaf mandarin (WLM) nucleotide diversity and genotype maps for three traditional mandarins (Ponkan mandarin (PKM), WLM, Huanglingmiao (HLM)) and three recent mandarin types (Clementine (CLM), W. Murcott mandarin (WMM), haploid Clementine reference (HCR)). For the haploid Clementine reference sequence (HCR), red and green segments indicate C.reticulata and C. maxima haplotypes, respectively. All five mandarin types show pummelo introgressions (blue or green segments). (c) Low acid pummelo (LAP) nucleotide diversity and genotype maps for two pummelos (LAP, Chandler pummelo (CHP)).
Figure 4
Figure 4. Mangshan mandarin is a species distinct from C. maxima and C. reticulata
(a) Midpoint-rooted neighbor-joining phylogenetic tree of citrus chloroplast genomes. (b) The frequency distributions of the pairwise sequence divergences (across 100 kb windows) between Mangshan mandarin (CMS) and C. maxima (green), CMS and C. reticulata (orange), C. reticulata and C. maxima (light blue), as well as the distinctly lower CMS intrinsic nucleotide diversity (dashed blue). (c) The first two coordinates of principal coordinate analysis of the citrus nuclear genomes, based on pairwise distances and the metric multidimensional scaling. The C. maxima - C. reticulata axis (Principle coordinate 1, 47.5% variance) separates pummelos (green) from mandarins (orange), with oranges (blue) lying in between; Principle coordinate 2 (19.6% of variance) separates CMS (purple) from the others.

Comment in

  • A genealogy of the citrus family.
    Velasco R, Licciardello C. Velasco R, et al. Nat Biotechnol. 2014 Jul;32(7):640-2. doi: 10.1038/nbt.2954. Nat Biotechnol. 2014. PMID: 25004231 No abstract available.

Similar articles

See all similar articles

Cited by 133 articles

See all "Cited by" articles

References

    1. Bové J. HUANGLONGBING: A DESTRUCTIVE, NEWLY-EMERGING, CENTURY-OLD DISEASE OF CITRUS. J. Plant Path. 2006;88:7–37.
    1. Reuther W, Webber HJ, Batchelor LD, editors. The Citrus Industry. Edn. 1. Vol. 1. Berkeley: University of California, Division of Agricultural Sciences; 1967.
    1. Spiegel-Roy P, Goldschmidt EE. Biology of citrus. Cambridge; New York: Cambridge University Press; 1996.
    1. Scora RW. On the history and origin of Citrus. Bull. Torrey Botanical Club. 1975;102:369–375.
    1. Barrett HC, Rhodes AM. A numerical taxonomic study of affinity relationships in cultivated citrus and its close relatives. Syst. Biol. 1976;1:105–136.

Publication types

Feedback