Jia-Xing Yue

Recent duplications dominate NBS-encoding gene expansion in two woody species

Most disease resistance genes in plants encode NBS-LRR proteins. However, in woody species, little is known about the evolutionary history of these genes. Here, we identified 459 and 330 respective NBS-LRRs in grapevine and poplar genomes. We subsequently investigated protein motif composition, phylogenetic relationships and physical locations. We found significant excesses of recent duplications in perennial species, compared with those of annuals, represented by rice and Arabidopsis. Consequently, we observed higher nucleotide identity among paralogs and a higher percentage of NBS-encoding genes positioned in numerous clusters in the grapevine and poplar. These results suggested that recent tandem duplication played a major role in NBS-encoding gene expansion in perennial species. These duplication events, together with a higher probability of recombination revealed in this study, could compensate for the longer generation time in woody perennial species e.g. duplication and recombination could serve to generate novel resistance specificities. In addition, we observed extensive species-specific expansion in TIR-NBS-encoding genes. Non-TIR-NBS-encoding genes were poly- or paraphyletic, i.e. genes from three or more plant species were nested in different clades, suggesting different evolutionary patterns between these two gene types.

Tracing the origin and evolutionary history of plant nucleotide‐binding site–leucine‐rich repeat (NBS‐LRR) genes

Plant disease resistance genes (R genes) encode proteins that function to monitor signals indicating pathogenic infection, thus playing a critical role in the plants defense system. Although many studies have been performed to explore the functional details of these important genes, their origin and evolutionary history remain unclear. In this study, focusing on the largest group of R genes, the nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes, we conducted an extensive genome-wide survey of 38 representative model organisms and obtained insights into the evolutionary stage and timing of NBS-LRR genes. Our data show that the two major domains, NBS and LRR, existed before the split of prokaryotes and eukaryotes but their fusion was observed only in land plant lineages. The Toll/interleukin-1 receptor (TIR) class of NBS-LRR genes probably had an earlier origin than its nonTIR counterpart. The similarities of the innate immune systems of plants and animals are likely to have been shaped by convergent evolution after their independent origins. Our findings start to unravel the evolutionary history of these important genes from the perspective of comparative genomics and also highlight the important role of reorganizing pre-existing building blocks in generating evolutionary novelties.

Hemichordate genomes and deuterostome origins

Acorn worms, also known as enteropneust (literally, ‘gut-breathing’) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal ‘gill’ slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.

Joint assembly and genetic mapping of the Atlantic horseshoe crab genome reveals ancient whole genome duplication

BackgroundHorseshoe crabs are marine arthropods with a fossil record extending back approximately 450 million years. They exhibit remarkable morphological stability over their long evolutionary history, retaining a number of ancestral arthropod traits, and are often cited as examples of “living fossils.” As arthropods, they belong to the Ecdysozoa, an ancient super-phylum whose sequenced genomes (including insects and nematodes) have thus far shown more divergence from the ancestral pattern of eumetazoan genome organization than cnidarians, deuterostomes and lophotrochozoans. However, much of ecdysozoan diversity remains unrepresented in comparative genomic analyses.ResultsHere we apply a new strategy of combined de novo assembly and genetic mapping to examine the chromosome-scale genome organization of the Atlantic horseshoe crab, Limulus polyphemus. We constructed a genetic linkage map of this 2.7 Gbp genome by sequencing the nuclear DNA of 34 wild-collected, full-sibling embryos and their parents at a mean redundancy of 1.1x per sample. The map includes 84,307 sequence markers grouped into 1,876 distinct genetic intervals and 5,775 candidate conserved protein coding genes.ConclusionsComparison with other metazoan genomes shows that the L. polyphemus genome preserves ancestral bilaterian linkage groups, and that a common ancestor of modern horseshoe crabs underwent one or more ancient whole genome duplications 300 million years ago, followed by extensive chromosome fusion. These results provide a counter-example to the often noted correlation between whole genome duplication and evolutionary radiations. The new, low-cost genetic mapping method for obtaining a chromosome-scale view of non-model organism genomes that we demonstrate here does not require laboratory culture, and is potentially applicable to a broad range of other species.

Genome-wide investigation reveals high evolutionary rates in annual model plants.

BackgroundRates of molecular evolution vary widely among species. While significant deviations from molecular clock have been found in many taxa, effects of life histories on molecular evolution are not fully understood. In plants, annual/perennial life history traits have long been suspected to influence the evolutionary rates at the molecular level. To date, however, the number of genes investigated on this subject is limited and the conclusions are mixed. To evaluate the possible heterogeneity in evolutionary rates between annual and perennial plants at the genomic level, we investigated 85 nuclear housekeeping genes, 10 non-housekeeping families, and 34 chloroplast genes using the genomic data from model plants including Arabidopsis thaliana and Medicago truncatula for annuals and grape (Vitis vinifera) and popular (Populus trichocarpa) for perennials.ResultsAccording to the cross-comparisons among the four species, 74-82% of the nuclear genes and 71-97% of the chloroplast genes suggested higher rates of molecular evolution in the two annuals than those in the two perennials. The significant heterogeneity in evolutionary rate between annuals and perennials was consistently found both in nonsynonymous sites and synonymous sites. While a linear correlation of evolutionary rates in orthologous genes between species was observed in nonsynonymous sites, the correlation was weak or invisible in synonymous sites. This tendency was clearer in nuclear genes than in chloroplast genes, in which the overall evolutionary rate was small. The slope of the regression line was consistently lower than unity, further confirming the higher evolutionary rate in annuals at the genomic level.ConclusionsThe higher evolutionary rate in annuals than in perennials appears to be a universal phenomenon both in nuclear and chloroplast genomes in the four dicot model plants we investigated. Therefore, such heterogeneity in evolutionary rate should result from factors that have genome-wide influence, most likely those associated with annual/perennial life history. Although we acknowledge current limitations of this kind of study, mainly due to a small sample size available and a distant taxonomic relationship of the model organisms, our results indicate that the genome-wide survey is a promising approach toward further understanding of the mechanism determining the molecular evolutionary rate at the genomic level.

Contrasting evolutionary genome dynamics between domesticated and wild yeasts

Structural rearrangements have long been recognized as an important source of genetic variation, with implications in phenotypic diversity and disease, yet their detailed evolutionary dynamics remain elusive. Here we use long-read sequencing to generate end-to-end genome assemblies for 12 strains representing major subpopulations of the partially domesticated yeast Saccharomyces cerevisiae and its wild relative Saccharomyces paradoxus. These population-level high-quality genomes with comprehensive annotation enable precise definition of chromosomal boundaries between cores and subtelomeres and a high-resolution view of evolutionary genome dynamics. In chromosomal cores, S. paradoxus shows faster accumulation of balanced rearrangements (inversions, reciprocal translocations and transpositions), whereas S. cerevisiae accumulates unbalanced rearrangements (novel insertions, deletions and duplications) more rapidly. In subtelomeres, both species show extensive interchromosomal reshuffling, with a higher tempo in S. cerevisiae. Such striking contrasts between wild and domesticated yeasts are likely to reflect the influence of human activities on structural genome evolution.

The Transcriptome of an Amphioxus, Asymmetron lucayanum, from the Bahamas: A Window into Chordate Evolution

Cephalochordates, the sister group of tunicates plus vertebrates, have been called “living fossils” due to their resemblance to fossil chordates from Cambrian strata. The genome of the cephalochordate Branchiostoma floridae shares remarkable synteny with vertebrates and is free from whole-genome duplication. We performed RNA sequencing from larvae and adults of Asymmetron lucayanum, a cephalochordate distantly related to B. floridae. Comparisons of about 430 orthologous gene groups among both cephalochordates and 10 vertebrates using an echinoderm, a hemichordate, and a mollusk as outgroups showed that cephalochordates are evolving more slowly than the slowest evolving vertebrate known (the elephant shark), with A. lucayanum evolving even more slowly than B. floridae. Against this background of slow evolution, some genes, notably several involved in innate immunity, stand out as evolving relatively quickly. This may be due to the lack of an adaptive immune system and the relatively high levels of bacteria in the inshore waters cephalochordates inhabit. Molecular dating analysis including several time constraints revealed a divergence time of ∼120 Ma for A. lucayanum and B. floridae. The divisions between cephalochordates and vertebrates, and that between chordates and the hemichordate plus echinoderm clade likely occurred before the Cambrian.

De novo yeast genome assemblies from MinION, PacBio and MiSeq platforms

Long-read sequencing technologies such as Pacific Biosciences and Oxford Nanopore MinION are capable of producing long sequencing reads with average fragment lengths of over 10,000 base-pairs and maximum lengths reaching 100,000 base- pairs. Compared with short reads, the assemblies obtained from long-read sequencing platforms have much higher contig continuity and genome completeness as long fragments are able to extend paths into problematic or repetitive regions. Many successful assembly applications of the Pacific Biosciences technology have been reported ranging from small bacterial genomes to large plant and animal genomes. Recently, genome assemblies using Oxford Nanopore MinION data have attracted much attention due to the portability and low cost of this novel sequencing instrument. In this paper, we re-sequenced a well characterized genome, the Saccharomyces cerevisiae S288C strain using three different platforms: MinION, PacBio and MiSeq. We present a comprehensive metric comparison of assemblies generated by various pipelines and discuss how the platform associated data characteristics affect the assembly quality. With a given read depth of 31X, the assemblies from both Pacific Biosciences and Oxford Nanopore MinION show excellent continuity and completeness for the 16 nuclear chromosomes, but not for the mitochondrial genome, whose reconstruction still represents a significant challenge.

Genome evolution across 1,011 Saccharomyces cerevisiae isolates

Large-scale population genomic surveys are essential to explore the phenotypic diversity of natural populations. Here we report the whole-genome sequencing and phenotyping of 1,011 Saccharomyces cerevisiae isolates, which together provide an accurate evolutionary picture of the genomic variants that shape the species-wide phenotypic landscape of this yeast. Genomic analyses support a single ‘out-of-China’ origin for this species, followed by several independent domestication events. Although domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates is mainly driven by the accumulation of single nucleotide polymorphisms. A common feature is the extensive loss of heterozygosity, which represents an essential source of inter-individual variation in this mainly asexual species. Most of the single nucleotide polymorphisms, including experimentally identified functional polymorphisms, are present at very low frequencies. The largest numbers of variants identified by genome-wide association are copy-number changes, which have a greater phenotypic effect than do single nucleotide polymorphisms. This resource will guide future population genomics and genotype–phenotype studies in this classic model system.Whole-genome sequencing of 1,011 natural isolates of the yeast Saccharomyces cerevisiae reveals its evolutionary history, including a single out-of-China origin and multiple domestication events, and provides a framework for genotype–phenotype studies in this model organism.

A histone H3K9M mutation traps histone methyltransferase Clr4 to prevent heterochromatin spreading

Histone lysine-to-methionine (K-to-M) mutations are associated with multiple cancers, and they function in a dominant fashion to block the methylation of corresponding lysines on wild type histones. However, their mechanisms of function are controversial. Here we show that in fission yeast, introducing the K9M mutation into one of the three histone H3 genes dominantly blocks H3K9 methylation on wild type H3 across the genome. In addition, H3K9M enhances the interaction of histone H3 tail with the H3K9 methyltransferase Clr4 in a SAM (S-adenosyl-methionine)-dependent manner, and Clr4 is trapped at nucleation sites to prevent its spreading and the formation of large heterochromatin domains. We further determined the crystal structure of an H3K9M peptide in complex with human H3K9 methyltransferase G9a and SAM, which reveales that the methionine side chain had enhanced van der Waals interactions with G9a. Therefore, our results provide a detailed mechanism by which H3K9M regulates H3K9 methylation. DOI: http://dx.doi.org/10.7554/eLife.17903.001