skip to main content


Title: Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication
Abstract

Domestication of the apple was mainly driven by interspecific hybridization. In the present study, we report the haplotype-resolved genomes of the cultivated apple (Malus domesticacv. Gala) and its two major wild progenitors,M. sieversiiandM. sylvestris. Substantial variations are identified between the two haplotypes of each genome. Inference of genome ancestry identifies ~23% of the Gala genome as of hybrid origin. Deep sequencing of 91 accessions identifies selective sweeps in cultivated apples that originated from either of the two progenitors and are associated with important domestication traits. Construction and analyses of apple pan-genomes uncover thousands of new genes, with hundreds of them being selected from one of the progenitors and largely fixed in cultivated apples, revealing that introgression of new genes/alleles is a hallmark of apple domestication through hybridization. Finally, transcriptome profiles of Gala fruits at 13 developmental stages unravel ~19% of genes displaying allele-specific expression, including many associated with fruit quality.

 
more » « less
Award ID(s):
1855585
NSF-PAR ID:
10205243
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Genetics
Volume:
52
Issue:
12
ISSN:
1061-4036
Page Range / eLocation ID:
p. 1423-1432
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Breeding of agricultural crops adapted to climate change and resistant to diseases and pests is hindered by a limited gene pool because of domestication and thousands of years of human selection. One way to increase genetic variation is chromosome-mediated gene transfer from wild relatives by cross hybridization. In the case of wheat ( Triticum aestivum ), the species of genus Aegilops are a particularly attractive source of new genes and alleles. However, during the evolution of the Aegilops and Triticum genera, diversification of the D-genome lineage resulted in the formation of diploid C, M, and U genomes of Aegilops . The extent of structural genome alterations, which accompanied their evolution and speciation, and the shortage of molecular tools to detect Aegilops chromatin hamper gene transfer into wheat. To investigate the chromosome structure and help develop molecular markers with a known physical position that could improve the efficiency of the selection of desired introgressions, we developed single-gene fluorescence in situ hybridization (FISH) maps for M- and U-genome progenitors, Aegilops comosa and Aegilops umbellulata , respectively. Forty-three ortholog genes were located on 47 loci in Ae. comosa and on 52 loci in Ae. umbellulata using wheat cDNA probes. The results obtained showed that M-genome chromosomes preserved collinearity with those of wheat, excluding 2 and 6M containing an intrachromosomal rearrangement and paracentric inversion of 6ML, respectively. While Ae. umbellulata chromosomes 1, 3, and 5U maintained collinearity with wheat, structural reorganizations in 2, 4, 6, and 7U suggested a similarity with the C genome of Aegilops markgrafii . To develop molecular markers with exact physical positions on chromosomes of Aegilops , the single-gene FISH data were validated in silico using DNA sequence assemblies from flow-sorted M- and U-genome chromosomes. The sequence similarity search of cDNA sequences confirmed 44 out of the 47 single-gene loci in Ae. comosa and 40 of the 52 map positions in Ae. umbellulata . Polymorphic regions, thus, identified enabled the development of molecular markers, which were PCR validated using wheat- Aegilops disomic chromosome addition lines. The single-gene FISH-based approach allowed the development of PCR markers specific for cytogenetically mapped positions on Aegilops chromosomes, substituting as yet unavailable segregating map. The new knowledge and resources will support the efforts for the introgression of Aegilops genes into wheat and their cloning. 
    more » « less
  2. 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
  3. Abstract

    Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks andN6-methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement.

     
    more » « less
  4. Abstract

    Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships.

    To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory byManduca sexta, and the attraction of a parasitoid wasp,Cotesia congregata.

    Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks.

    Plant cultivars had different levels of resistance to herbivory byM. sexta, but this did not depend on plant domestication or soil type. The parasitoidC. congregatawas primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil.

    Synthesis.These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

     
    more » « less
  5. Abstract

    It remains a major challenge to identify the genes and mutations that lead to plant sexual differentiation. Here, we study the structure and evolution of the sex-determining region (SDR) inVitisspecies. We report an improved, chromosome-scale Cabernet Sauvignon genome sequence and the phased assembly of nine wild and cultivated grape genomes. By resolving twentyVitisSDR haplotypes, we compare male, female, and hermaphrodite haplotype structures and identify sex-linked regions. Coupled with gene expression data, we identify a candidate male-sterility mutation in theVviINP1gene and potential female-sterility function associated with the transcription factorVviYABBY3. Our data suggest that dioecy has been lost during domestication through a rare recombination event between male and female haplotypes. This work significantly advances the understanding of the genetic basis of sex determination inVitisand provides the information necessary to rapidly identify sex types in grape breeding programs.

     
    more » « less