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. 2020 Mar 6;21(1):60.
doi: 10.1186/s13059-020-01959-8.

The Genome Evolution and Domestication of Tropical Fruit Mango

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Free PMC article

The Genome Evolution and Domestication of Tropical Fruit Mango

Peng Wang et al. Genome Biol. .
Free PMC article

Abstract

Background: Mango is one of the world's most important tropical fruits. It belongs to the family Anacardiaceae, which includes several other economically important species, notably cashew, sumac and pistachio from other genera. Many species in this family produce family-specific urushiols and related phenols, which can induce contact dermatitis.

Results: We generate a chromosome-scale genome assembly of mango, providing a reference genome for the Anacardiaceae family. Our results indicate the occurrence of a recent whole-genome duplication (WGD) event in mango. Duplicated genes preferentially retained include photosynthetic, photorespiration, and lipid metabolic genes that may have provided adaptive advantages to sharp historical decreases in atmospheric carbon dioxide and global temperatures. A notable example of an extended gene family is the chalcone synthase (CHS) family of genes, and particular genes in this family show universally higher expression in peels than in flesh, likely for the biosynthesis of urushiols and related phenols. Genome resequencing reveals two distinct groups of mango varieties, with commercial varieties clustered with India germplasms and demonstrating allelic admixture, and indigenous varieties from Southeast Asia in the second group. Landraces indigenous in China formed distinct clades, and some showed admixture in genomes.

Conclusions: Analysis of chromosome-scale mango genome sequences reveals photosynthesis and lipid metabolism are preferentially retained after a recent WGD event, and expansion of CHS genes is likely associated with urushiol biosynthesis in mango. Genome resequencing clarifies two groups of mango varieties, discovers allelic admixture in commercial varieties, and shows distinct genetic background of landraces.

Keywords: Germplasm; Mango genome; Photosynthesis; Urushiol; Whole-genome duplication.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Overview of the mango (Mangifera indica) genome assembly. The outer layer of colored blocks is a circular representation of the 20 pseudomolecules, with thick mark labeling each 5 Mb. The distribution of genetic markers mapped to mango chromosomes is shown in (A). Repeat density (B) and gene density (C) are calculated in 100-kb windows sliding in 10-kb steps. Tandem duplicated genes are displayed in (D). Genes involved in disease resistance (E), pigment-related metabolisms (F, yellow lines represent carotenoid synthesis genes, green lines represent chl metabolism genes and red lines represent anthocyanin synthesis genes), lipid metabolism (G, red lines represent genes participant in the synthesis of triacylglycerol, sphingolipid, phospholipid and mitochondrial lipopolysaccharide, phospholipid signaling, and lipid trafficking; the green lines represent the rest lipid metabolism genes) and photosynthesis related genes (H, red lines represent photosystem genes, black lines represent the Calvin cycle genes, and green lines represent genes participant in sucrose and starch synthesis, glycolysis, and Krebs cycle) are also displayed. Transcription factors are shown in (I). The innermost layer shows inter-chromosomal synteny, with the red links representing syntenic blocks retained after a recent WGD in mango genome, and the gray links representing homologs as results of older WGD
Fig. 2
Fig. 2
A recent whole genome duplication and resulted gene fate in mango genome. (a) Inferred phylogenetic tree across 12 plant species including mango. Estimated WGD events wereindicated with circles. (b) Frequency distributions of synonymous substitution rates (Ks) betweenhomologous gene pairs in syntenic blocks of mango-mango, mango-orange, mango-longan andorange-longan. (c) Distribution of expressional correlation coefficient of syntenic homologousgene pairs retained from recent WGD and ancient WGD in mango genome. (d) Enrichment ofmetabolic genes retained after the recent WGD of mango genome. The vertical dashed linerepresents average percentage of genes retained after the recent WGD
Fig. 3
Fig. 3
Expansion of genes in metabolism of flavonoids, lipids, chlorophylls and terpenoids. (a) Gene family analysis showing expansion of genes in flavonoid biosynthesis, lipid metabolism, chlorophyll metabolism and isoprenoid biosynthesis, including CHS family. Numbers showing in cells represent genes counting of each family in each species. (b) Gene structure of a typical CHS peptide (here shows mango gene Mi07g07250). The blue and red blocks represent two conserved domains PF00195.15 and PF02797.11, respectively, and the red circles suggest three conserved residues, Cysteine, Histidine and Asparagine, respectively, within the sequence. (c) Topology of phylogenetic tree of genes containing conserved domains PF00195.15 and PF02797.11 from mango, sweet orange and Arabidopsis. CHS-encoding genes are classified in a distinctive class, here named CHS. (d) The expression pattern of CHS genes in mango cultivars. Unexpressed genes were not showed in this figure. (e) Macrosynteny and microsynteny among mango chr.3, orange chr. 9 and mango chr. 7. Top: macrosynteny patterns among mango chr.3, orange chr. 9 and mango chr. 7. Co-synteny regions are linked with grey belts, except synteny of the regions harboring CHS genes, which are highlighted with a red belt. Bottom: microsynteny of the regions harboring CHS genes among the three chr. The CHS genes are represented by triangles, and are linked with red lines
Fig. 4
Fig. 4
Expression of genes in chlorophyll degradation and anthocyanin biosynthesis in mango fruits. (a) Demonstration of peel colors of three representative mango varieties. Peel of developing fruit of Hongyu is green, while that of ripe fruit is yellow; peel of Guire-82 keeps green even when ripen; peel of Sensation demonstrates red color. (b) Expression of genes in chlorophyll degradation pathway in peel and flesh of Hongyu fruits as well as peel of Guire-82. (c) Expression of genes in anthocyanin biosynthesis in peel and flesh of Sensation fruits, as well as peels of Hongyu and Guire-82
Fig. 5
Fig. 5
Genomic diversity of M. indica varieties and relatives within Mangifera. 49 M. indica germplasms and 4 otherspecies in the genus of Mangifera were sampled for the analyses. (a) PCA analysis of the samples using SNP markers. The three groups indicated by phylogenetic (b) and STRUCTURE (k=3) (c) analyses were circled, respectively. Germplasms with different backgrounds are represented with dots with different shapes and colors. (b) Neighbor-joining phylogenetic tree of the samples in polar layout based on SNPs. Clades of the three major groups are indicated with different colors as indicated in STRUCTURE analysis (k=3). Tips of outgroup germplasms are indicated with green hollow blocks. Tips of traditional and commercial varieties are labeled with filled rounds, and those representing landraces are suggested as hollow circular forms. Traditional varieties and commercial cultivars without admixture are labeled in red, and germplasms representing Southeast Asia varieties and landraces are in yellow, while those with allele admixture are in blue. (c) STRUCTURE analysis of the samples, with each color representing one population, and the length of each color segment in each vertical bar representing the proportion contributed by ancestral populations. On the right is assumed number of clusters (k), and below is the name or origin of the samples. (d) Circos demonstration of genetic diversity. Outer circle represents 20 pseudo-molecules of mango genome. i, contents of repetitive elements; iia- iic, nucleotide diversity (π) of other Mangifera species, varieties of Southeast Asia and India germplasms, respectively. iiia-iiic, population differentiation (FST) levels of other Mangifera species vs. germplasms of Southeast Asia, other Mangifera species vs. India germplasms, and those of Southeast Asia vs. India, respectively

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