Genomes of cultivated and wild Capsicum species provide insights into pepper domestication and population differentiation

Abstract

Pepper (Capsicum spp.) is one of the earliest cultivated crops and includes five domesticated species, C. annuum var. annuum, C. chinense, C. frutescens, C. baccatum var. pendulum and C. pubescens. Here, we report a pepper graph pan-genome and a genome variation map of 500 accessions from the five domesticated Capsicum species and close wild relatives. We identify highly differentiated genomic regions among the domesticated peppers that underlie their natural variations in flowering time, characteristic flavors, and unique resistances to biotic and abiotic stresses. Domestication sweeps detected in C. annuum var. annuum and C. baccatum var. pendulum are mostly different, and the common domestication traits, including fruit size, shape and pungency, are achieved mainly through the selection of distinct genomic regions between these two cultivated species. Introgressions from C. baccatum into C. chinense and C. frutescens are detected, including those providing genetic sources for various biotic and abiotic stress tolerances.

Fig. 1. Phylogeny and population structure of Capsicum accessions.

a Geographical distribution of the core pepper accessions (after taxonomy correction). The size of the pie corresponds to the total number of accessions from the selected geographical region. For C. galapagoense, only one accession with unknown geographic information was available and is not presented on the map. b Maximum likelihood phylogenetic tree and population structure of the core pepper accessions. c, d Principal component (PC) analysis, PC1 versus PC2 (c) and PC2 versus PC3 (d), of the core pepper accessions.

Fig. 2. Population differentiation and history of Capsicum species.

a Fixation index (F_ST) between different pepper populations. For each comparison, all F_ST values generated from 100 permutations were lower than the empirical F_ST value. b Total size of highly differentiated genome regions (top 1% F_ST) among the five domesticated Capsicum species. c Number of genes within the highly differentiated regions. d UpSet plot of common and unique genes within the differentiated regions among the five domesticated Capsicum species. e History of the effective population size of different pepper groups. f Linkage disequilibrium (LD) decay pattern of different pepper groups. g Boxplots of nucleotide diversity (π) for different pepper groups. For each box plot, the lower and upper bounds of the box indicate the first and third quartiles, respectively, and the center line indicates the median. The numbers of windows (n) for PUB, CHA, BAB, BAP, GLA, ANN, FRU and CHN are 28,893, 28,672, 28,736, 29,061, 29,007, 29,141, 29,242, 29,189, respectively. Note, π values could be overestimated due to the sub-sampling using GenoCore. PUB, C. pubescens; CHA, C. chacoense; BAB, C. baccatum var. baccatum; BAP, C. baccatum var. pendulum; FRU, C. frutescens; CHN, C. chinense; GLA, C. annuum var. glabriusculum; ANN, C. annuum var. annuum. Detailed gene information is provided in Supplementary Data 5.

Fig. 3. Convergent and divergent domestication of C. annuum var. annuum and C. baccatum var. pendulum.

a Fruits of representative wild and domesticated C. annuum and C. baccatum accessions with diverse shapes. Vertical bar represents 1 cm. b Fruit length, fruit width and fruit shape index in wild and domesticated C. annuum and C. baccatum accessions. Significant difference between groups was assessed using the two-tailed Student’s test. c, d Selective sweeps in C. annuum var. annuum (c) and C. baccatum var. pendulum (d). Fruit weight, shape, and pungency-related genes (in bold) and QTLs are presented in pink, orange, and cyan, respectively. Dashed horizontal lines indicate the top 5% Composite likelihood ratio (CLR) scores. Red dots correspond to selective sweeps identified in both C. annuum var. annuum and C. baccatum var. pendulum, and orange, dark green, dark orange and purple dots indicate CLR scores on different chromosomes. e Common and specific genome regions and genes under selection during C. annuum var. annuum and C. baccatum var. pendulum domestication. f, g Manhattan plots of genome-wide association studies of fruit shape of C. annuum (f) and C. baccatum (g) accessions. Red and blue horizontal lines indicate the Bonferroni-corrected significance thresholds of GWAS at α = 0.05 and α = 1, respectively. h Nucleotide diversity (π) and allele conservation of C. baccatum var. baccatum and C. baccatum var. pendulum accessions with fruit shape index >4 (the elongated dedo-de-moça type) and those with fruit shape index <1.2 (the cambuci type). GLA, C. annuum var. glabriusculum; ANN, C. annuum var. annuum; BAB, C. baccatum var. baccatum; BAP, C. baccatum var. pendulum. Detailed information on genes and QTLs is provided in Supplementary Data 6. Source data are provided as a Source Data file.

Fig. 4. Introgressions among the Capsicum species.

a Phylogenetic structure and gene flow detected between the Baccatum and the Annuum clades. The red arrow line indicates the direction of gene flow. b Four-taxon topology ((P1,P2),P3,O) used in the ABBA-BABA model to detect the degree of introgression (fd) and proportion of introgression across the whole genome (PGI) between C. baccatum (var. baccatum and var. pendulum) and the subgroup of the Annuum clade including C. frutescens and C. chinense. c Degree of introgression (fd) from C. baccatum to C. chinense and C. frutescens across the pepper genome. The top five strongest introgression signals are indicated by black arrows. Dashed horizontal lines indicate the top 1% fd. d Nucleotide diversity (π) of the genome region at the end of chromosome 6 containing the strongest introgression signal. e Introgression from C. baccatum to C. chinense and C. frutescens at the end of chromosome 6. The dark red color represents alleles prevalent in C. baccatum accessions (allele frequency ≥ 0.8). f LD decay patterns of the introgressed region shown in (e). PUB, C. pubescens; BAB, C. baccatum var. baccatum; BAP, C. baccatum var. pendulum; FRU, C. frutescens; CHN, C. chinense; ANN, C. annuum var. annuum.

Fig. 5. Domestication, differentiation and introgression of the Capsicum species.

Representative fruits are presented for each species/group. Circles and squares represent the domesticated and wild types, respectively. Dark red, light brown and brown represent Pubescens, Baccatum and Annuum clades, respectively. Genes related to population differentiation (dashed white arrows) and introgression (purple arrow) are indicated in white and purple colors, respectively. Selected genes (in bold) and QTLs related to fruit shape, fruit size/weight and pungency during pepper domestication (green arrows) are highlighted in pink, green and cyan, respectively. PUB, C. pubescens; CHA, C. chacoense; BAB, C. baccatum var. baccatum; BAP, C. baccatum var. pendulum; FRU, C. frutescens; CHN, C. chinense; GLA, C. annuum var. glabriusculum; ANN, C. annuum var. annuum. Genes/QTLs are the same as those shown in Figs. 2 and 3 and Supplementary Fig. 8.