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The merger of divergent genomes, via hybridization or allopolyploidization, frequently results in a ‘genomic shock’ that induces a series of rapid genetic and epigenetic modifications as a result of conflicts between parental genomes. This conflict among the subgenomes routinely leads one subgenome to become dominant over the other subgenome(s), resulting in subgenome biases in gene content and expression. Recent advances in methods to analyze hybrid and polyploid genomes with comparisons to extant parental progenitors have allowed for major strides in understanding the mechanistic basis for subgenome dominance. In particular, our understanding of the role that homoeologous exchange might play in subgenome dominance and genome evolution is quickly growing. Here we describe recent discoveries uncovering the underlying mechanisms and provide a framework to predict subgenome dominance in hybrids and allopolyploids with far-reaching implications for agricultural, ecological, and evolutionary research.

Mutualistic symbioses between eukaryotes and beneficial microorganisms of their microbiome play an essential role in nutrition, protection against disease, and development of the host. However, the impact of beneficial symbionts on the evolution of host genomes remains poorly characterized. Here we used the independent loss of the most widespread plant-microbe symbiosis, arbuscular mycorrhization (AM), as a model to address this question. Using a large phenotypic approach and phylogenetic analyses, we present evidence that loss of AM symbiosis correlates with the loss of many symbiotic genes in the Arabidopsis lineage (Brassicales). Then, by analyzing the genome and/or transcriptomes of nine other phylogenetically divergent non-host plants, we show that this correlation occurred in a convergent manner in four additional plant lineages, demonstrating the existence of an evolutionary pattern specific to symbiotic genes. Finally, we use a global comparative phylogenomic approach to track this evolutionary pattern among land plants. Based on this approach, we identify a set of 174 highly conserved genes and demonstrate enrichment in symbiosis-related genes. Our findings are consistent with the hypothesis that beneficial symbionts maintain purifying selection on host gene networks during the evolution of entire lineages.

Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry ( Fragaria   ×   ananassa ) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry. Chromosome-scale assembly for the cultivated octoploid strawberry ( Fragaria × ananassa ) uncovers the origin and evolutionary processes that shaped this complex allopolyploid, providing a useful resource for genome-wide analyses and molecular breeding.

• Plants produce a range of volatile organic compounds (VOCs), some of which are perceived by the human olfactory system, contributing to a myriad flavors. Despite the importance of flavor for consumer preference, most plant breeding programs have neglected it, mainly because of the costs of phenotyping and the complexity of disentangling the role of VOCs in human perception. • To develop molecular breeding tools aimed at improving fruit flavor, we carried out target genotyping of and VOC extraction from a blueberry population. Metabolite genome-wide association analysis was used to elucidate the genetic architecture, while predictive models were tested to prove that VOCs can be accurately predicted using genomic information. A historical sensory panel was considered to assess how the volatiles influenced consumers. • By gathering genomics, metabolomics, and the sensory panel, we demonstrated that VOCs are controlled by a few major genomic regions, some of which harbor biosynthetic enzyme-coding genes; can be accurately predicted using molecular markers; and can enhance or decrease consumers’ overall liking. • Here we emphasized how the understanding of the genetic basis and the role of VOCs in consumer preference can assist breeders in developing more flavorful cultivars at a more inexpensive and accelerated pace.

Teff ( Eragrostis tef ) is a cornerstone of food security in the Horn of Africa, where it is prized for stress resilience, grain nutrition, and market value. Here, we report a chromosome-scale assembly of allotetraploid teff (variety Dabbi) and patterns of subgenome dynamics. The teff genome contains two complete sets of homoeologous chromosomes, with most genes maintaining as syntenic gene pairs. TE analysis allows us to estimate that the teff polyploidy event occurred ~1.1 million years ago (mya) and that the two subgenomes diverged ~5.0 mya. Despite this divergence, we detect no large-scale structural rearrangements, homoeologous exchanges, or biased gene loss, in contrast to many other allopolyploids. The two teff subgenomes have partitioned their ancestral functions based on divergent expression across a diverse expression atlas. Together, these genomic resources will be useful for accelerating breeding of this underutilized grain crop and for fundamental insights into polyploid genome evolution. Teff is an indigenous cereal critical to food security in the Horn of Africa. Here, the authors report an improved genome assembly and observe the surprisingly low levels of large-scale structural rearrangement, homoeologous exchanges, or bias gene loss after the formation of this tetraploid species.

There is an increasing awareness that as a result of structural variation, a reference sequence representing a genome of a single individual is unable to capture all of the gene repertoire found in the species. A large number of genes affected by presence/absence and copy number variation suggest that it may contribute to phenotypic and agronomic trait diversity. Here we show by analysis of the Brassica oleracea pangenome that nearly 20% of genes are affected by presence/absence variation. Several genes displaying presence/absence variation are annotated with functions related to major agronomic traits, including disease resistance, flowering time, glucosinolate metabolism and vitamin biosynthesis. Brassica oleracea is a single species that includes diverse crops such as cabbage, broccoli and Brussels sprouts. Here, the authors identify genes not captured in existing B. oleracea reference genomes by the assembly of a pangenome and show variations in gene content that may be related to important agronomic traits

Oropetium thomaeum is a resurrection plant that can survive extreme water stress through desiccation to complete dryness, providing a model for drought tolerance; here, whole-genome sequencing and assembly of the Oropetium genome using single-molecule real-time sequencing is reported. A genomic model for drought tolerance Oropetium thomaeum is a resurrection plant that can endure extreme water stress through desiccation to complete dryness whilst retaining the ability to revive when water is available, providing a model for drought tolerance. These authors report whole-genome sequencing and assembly of the O. thomaeum genome, using only single-molecule real-time (SMRT) long-read sequencing. Understanding the genomic mechanisms of extreme desiccation tolerance in resurrection plants such as Oropetium may provide targets for engineering drought and stress tolerance in crop plants. Plant genomes, and eukaryotic genomes in general, are typically repetitive, polyploid and heterozygous, which complicates genome assembly 1 . The short read lengths of early Sanger and current next-generation sequencing platforms hinder assembly through complex repeat regions, and many draft and reference genomes are fragmented, lacking skewed GC and repetitive intergenic sequences, which are gaining importance due to projects like the Encyclopedia of DNA Elements (ENCODE) 2 . Here we report the whole-genome sequencing and assembly of the desiccation-tolerant grass Oropetium thomaeum . Using only single-molecule real-time sequencing, which generates long (>16 kilobases) reads with random errors, we assembled 99% (244 megabases) of the Oropetium genome into 625 contigs with an N50 length of 2.4 megabases. Oropetium is an example of a ‘near-complete’ draft genome which includes gapless coverage over gene space as well as intergenic sequences such as centromeres, telomeres, transposable elements and rRNA clusters that are typically unassembled in draft genomes. Oropetium has 28,466 protein-coding genes and 43% repeat sequences, yet with 30% more compact euchromatic regions it is the smallest known grass genome. The Oropetium genome demonstrates the utility of single-molecule real-time sequencing for assembling high-quality plant and other eukaryotic genomes, and serves as a valuable resource for the plant comparative genomics community.

Brassicaceae is one of the most diverse and economically valuable angiosperm families with widely cultivated vegetable crops and scientifically important model plants, such as Arabidopsis thaliana. The evolutionary history, ecological, morphological, and genetic diversity, and abundant resources and knowledge of Brassicaceae make it an excellent model family for evolutionary studies. Recent phylogenetic analyses of the family revealed three major lineages (I, II, and III), but relationships among and within these lineages remain largely unclear. Here, we present a highly supported phylogeny with six major clades using nuclear markers from newly sequenced transcriptomes of 32 Brassicaceae species and large data sets from additional taxa for a total of 55 species spanning 29 out of 51 tribes. Clade A consisting of Lineage I and Macropodium nivale is sister to combined Clade B (with Lineage II and others) and a new Clade C. The ABC clade is sister to Clade D with species previously weakly associated with Lineage II and Clade E (Lineage III) is sister to the ABCD clade. Clade F (the tribe Aethionemeae) is sister to the remainder of the entire family. Molecular clock estimation reveals an early radiation of major clades near or shortly after the Eocene–Oligocene boundary and subsequent nested divergences of several tribes of the previously polytomous Expanded Lineage II. Reconstruction of ancestral morphological states during the Brassicaceae evolution indicates prevalent parallel (convergent) evolution of several traits over deep times across the entire family. These results form a foundation for future evolutionary analyses of structures and functions across Brassicaceae.

Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant, having retained more genes and being more highly expressed, a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of emergence of subgenome dominance, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, <140-year-old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and progenitor species (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are reduced in regions near genes and within TEs in the first-generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and recessive subgenomes in the natural allopolyploid. Subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following hybridization. These findings provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events and may also contribute to uncovering the mechanistic basis of heterosis and subgenome dominance.

Cultivated strawberry (Fragaria × ananassa) is one of our youngest domesticates, originating in early eighteenth-century Europe from spontaneous hybrids between wild allo-octoploid species (Fragaria chiloensis and Fragaria virginiana). The improvement of horticultural traits by 300 years of breeding has enabled the global expansion of strawberry production. Here, we describe the genomic history of strawberry domestication from the earliest hybrids to modern cultivars. We observed a significant increase in heterozygosity among interspecific hybrids and a decrease in heterozygosity among domesticated descendants of those hybrids. Selective sweeps were found across the genome in early and modern phases of domestication—59–76% of the selectively swept genes originated in the three less dominant ancestral subgenomes. Contrary to the tenet that genetic diversity is limited in cultivated strawberry, we found that the octoploid species harbor massive allelic diversity and that F. × ananassa harbors as much allelic diversity as either wild founder. We identified 41.8 M subgenome-specific DNA variants among resequenced wild and domesticated individuals. Strikingly, 98% of common alleles and 73% of total alleles were shared between wild and domesticated populations. Moreover, genome-wide estimates of nucleotide diversity were virtually identical in F. chiloensis,F. virginiana, and F. × ananassa (π = 0.0059–0.0060). We found, however, that nucleotide diversity and heterozygosity were significantly lower in modern F. × ananassa populations that have experienced significant genetic gains and have produced numerous agriculturally important cultivars.