skip to main content

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

Pepper (Capsicumspp.) is one of the earliest cultivated crops and includes five domesticated species,C. annuumvar.annuum,C. chinense,C. frutescens,C. baccatumvar.pendulumandC. pubescens. Here, we report a pepper graph pan-genome and a genome variation map of 500 accessions from the five domesticatedCapsicumspecies 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 inC. annuumvar.annuumandC. baccatumvar.pendulumare 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 fromC. baccatumintoC. chinenseandC. frutescensare detected, including those providing genetic sources for various biotic and abiotic stress tolerances.

more » « less
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; « less
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Communications
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The two cultivated allopolyploid cottons,Gossypium hirsutumandGossypium barbadense, represent a remarkable example of parallel independent domestication, both involving dramatic morphological transformations under selection from wild perennial plants to annualized row crops. Deep resequencing of 643 newly sampled accessions spanning the wild‐to‐domesticated continuum of both species, and their allopolyploid relatives, are combined with existing data to resolve species relationships and elucidate multiple aspects of their parallel domestication. It is confirmed that wildG. hirsutumandG. barbadensewere initially domesticated in the Yucatan Peninsula and NW South America, respectively, and subsequently spread under domestication over 4000–8000 years to encompass most of the American tropics. A robust phylogenomic analysis of infraspecific relationships in each species is presented, quantify genetic diversity in both, and describe genetic bottlenecks associated with domestication and subsequent diffusion. As these species became sympatric over the last several millennia, pervasive genome‐wide bidirectional introgression occurred, often with striking asymmetries involving the two co‐resident genomes of these allopolyploids. Diversity scans revealed genomic regions and genes unknowingly targeted during domestication and additional subgenomic asymmetries. These analyses provide a comprehensive depiction of the origin, divergence, and adaptation of cotton, and serve as a rich resource for cotton improvement.

    more » « less
  2. Abstract A-genome diploid wheats represent the earliest domesticated and cultivated wheat species in the Fertile Crescent and include the donor of the wheat A sub-genome. The A-genome species encompass the cultivated einkorn (Triticum monococcum L. subsp. monococcum), wild einkorn (T. monococcum L. subsp. aegilopoides (Link) Thell.), and Triticum urartu. We evaluated the collection of 930 accessions in the Wheat Genetics Resource Center (WGRC) using genotyping by sequencing and identified 13,860 curated single-nucleotide polymorphisms. Genomic analysis detected misclassified and genetically identical (>99%) accessions, with most of the identical accessions originating from the same or nearby locations. About 56% (n = 520) of the WGRC A-genome species collections were genetically identical, supporting the need for genomic characterization for effective curation and maintenance of these collections. Population structure analysis confirmed the morphology-based classifications of the accessions and reflected the species geographic distributions. We also showed that T. urartu is the closest A-genome diploid to the A-subgenome in common wheat (Triticum aestivum L.) through phylogenetic analysis. Population analysis within the wild einkorn group showed three genetically distinct clusters, which corresponded with wild einkorn races α, β, and γ described previously. The T. monococcum genome-wide FST scan identified candidate genomic regions harboring a domestication selection signature at the Non-brittle rachis 1 (Btr1) locus on the short arm of chromosome 3Am at ∼70 Mb. We established an A-genome core set (79 accessions) based on allelic diversity, geographical distribution, and available phenotypic data. The individual species core set maintained at least 79% of allelic variants in the A-genome collection and constituted a valuable genetic resource to improve wheat and domesticated einkorn in breeding programs. 
    more » « less
  3. Summary

    Humans have domesticated diverse species from across the plant kingdom, yet much of our foundational knowledge of domestication has come from studies investigating relatively few of the most important annual food crops. Here, we examine the impacts of domestication on genetic diversity in a tropical perennial fruit species, mango (Mangifera indica).

    We used restriction site associatedDNAsequencing to generate genomic single nucleotide polymorphism (SNP) data from 106 mango cultivars from seven geographical regions along with 52 samples of closely related species and unidentified cultivars to identify centers of mango genetic diversity and examine how post‐domestication dispersal shaped the geographical distribution of diversity.

    We identify two gene pools of cultivated mango, representing Indian and Southeast Asian germplasm. We found no significant genetic bottleneck associated with the introduction of mango into new regions of the world. By contrast, we show that mango populations in introduced regions have elevated levels of diversity.

    Our results suggest that mango has a more complex history of domestication than previously supposed, perhaps including multiple domestication events, hybridization and regional selection. Our work has direct implications for mango breeding and genebank management, and also builds on recent efforts to understand how woody perennial crops respond to domestication.

    more » « less
  4. null (Ed.)
    Salivary glucose oxidase (GOX) is one of the most abundant salivary proteins in generalist caterpillar Helicoverpa zea. GOX has been hypothesized to benefit H. zea by modulating direct defense responses of plants. Although the function of this protein has been studied, its role remains unclear. The study aims to test the hypothesis that GOX induces similar defensive responses among Solanaceous plants, and has similar consequences for larval performance of H. zea. Using six different plants in Solanaceae, including tomato (Solanum lycopersicum cv. Better Boy and S. lycopersicum var. cerasiforme), bell pepper (Capsicum annuum cv. Revolution), habanero pepper (Capsicum chinense), tomatillo (Physalis philadelphica cv. Tamayo), and tobacco (N. benthamiana), we tested the impact of GOX on induction of two common defense proteins, trypsin protease inhibitors (TPI) and polyphenol oxidases (PPO), and on relative growth rate of H. zea larvae. We found that GOX specifically induced TPI activity in tomato and habanero pepper, and the level of defense protein depended on leaf location. In addition, prior application of GOX did not increase the performance of H. zea in any plant tested. Changes in performance in tomato and habanero pepper matched the induction of TPI. In summary, our findings indicate that GOX induces similar defense responses in some Solanacean plants, but largely depends on species/genotype of plant, and that the presence of GOX did not benefit larval H. zea by modulating direct defense responses of plants. Other mechanisms must be involved in driving the evolution of this salivary protein. 
    more » « less
  5. Abstract The organization of chromatin into self-interacting domains is universal among eukaryotic genomes, though how and why they form varies considerably. Here we report a chromosome-scale reference genome assembly of pepper ( Capsicum annuum ) and explore its 3D organization through integrating high-resolution Hi-C maps with epigenomic, transcriptomic, and genetic variation data. Chromatin folding domains in pepper are as prominent as TADs in mammals but exhibit unique characteristics. They tend to coincide with heterochromatic regions enriched with retrotransposons and are frequently embedded in loops, which may correlate with transcription factories. Their boundaries are hotspots for chromosome rearrangements but are otherwise depleted for genetic variation. While chromatin conformation broadly affects transcription variance, it does not predict differential gene expression between tissues. Our results suggest that pepper genome organization is explained by a model of heterochromatin-driven folding promoted by transcription factories and that such spatial architecture is under structural and functional constraints. 
    more » « less