Mating system shifts and transposable element evolution in the plant genus Capsella

Background

Despite having predominately deleterious fitness effects, transposable elements (TEs) are major constituents of eukaryote genomes in general and of plant genomes in particular. Although the proportion of the genome made up of TEs varies at least four-fold across plants, the relative importance of the evolutionary forces shaping variation in TE abundance and distributions across taxa remains unclear. Under several theoretical models, mating system plays an important role in governing the evolutionary dynamics of TEs. Here, we use the recently sequenced Capsella rubella reference genome and short-read whole genome sequencing of multiple individuals to quantify abundance, genome distributions, and population frequencies of TEs in three recently diverged species of differing mating system, two self-compatible species (C. rubella and C. orientalis) and their self-incompatible outcrossing relative, C. grandiflora.

Results

We detect different dynamics of TE evolution in our two self-compatible species; C. rubella shows a small increase in transposon copy number, while C. orientalis shows a substantial decrease relative to C. grandiflora. The direction of this change in copy number is genome wide and consistent across transposon classes. For insertions near genes, however, we detect the highest abundances in C. grandiflora. Finally, we also find differences in the population frequency distributions across the three species.

Conclusion

Overall, our results suggest that the evolution of selfing may have different effects on TE evolution on a short and on a long timescale. Moreover, cross-species comparisons of transposon abundance are sensitive to reference genome bias, and efforts to control for this bias are key when making comparisons across species.

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A new type of specialized morphophysiological dormancy and seed storage behaviour in Hydatellaceae, an early-divergent angiosperm family

Background and Aims

Recent phylogenetic analysis has placed the aquatic family Hydatellaceae as an early-divergent angiosperm. Understanding seed dormancy, germination and desiccation tolerance of Hydatellaceae will facilitate ex situ conservation and advance hypotheses regarding angiosperm evolution.

Methods

Seed germination experiments were completed on three species of south-west Australian Hydatellaceae, Trithuria austinensis, T. bibracteata and T. submersa, to test the effects of temperature, light, germination stimulant and storage. Seeds were sectioned to examine embryo growth during germination in T. austinensis and T. submersa.

Key Results

Some embryo growth and cell division in T. austinensis and T. submersa occurred prior to the emergence of an undifferentiated embryo from the seed coat (‘germination’). Embryo differentiation occurred later, following further growth and a 3- to 4-fold increase in the number of cells. The time taken to achieve 50 % of maximum germination for seeds on water agar was 50, 35 and 37 d for T. austinensis, T bibracteata and T. submersa, respectively.

Conclusions

Seeds of Hydatellaceae have a new kind of specialized morphophysiological dormancy in which neither root nor shoot differentiates until after the embryo emerges from the seed coat. Seed biology is discussed in relation to early angiosperm evolution, together with ex situ conservation of this phylogenetically significant group.     

The mitochondrial genome of the chimpanzee louse,Pediculus schaeffi: insights into the process of mitochondrial genome fragmentation in the blood-sucking lice of great apes

Background

Blood-sucking lice in the genera Pediculus and Pthirus are obligate ectoparasites of great apes. Unlike most bilateral animals, which have 37 mitochondrial (mt) genes on a single circular chromosome, the sucking lice of humans have extensively fragmented mt genomes. The head louse, Pediculus capitis, and the body louse, Pe. humanus, have their 37 mt genes on 20 minichromosomes. The pubic louse, Pthirus pubis, has its 34 mt genes known on 14 minichromosomes. To understand the process of mt genome fragmentation in the sucking lice of great apes, we sequenced the mt genome of the chimpanzee louse, Pe. schaeffi, and compared it with the three human lice.

Results

We identified all of the 37 mt genes typical of bilateral animals in the chimpanzee louse; these genes are on 18 types of minichromosomes. Seventeen of the 18 minichromosomes of the chimpanzee louse have the same gene content and gene arrangement as their counterparts in the human head louse and the human body louse. However, five genes, cob, trnS₁, trnN, trnE and trnM, which are on three minichromosomes in the human head louse and the human body louse, are together on one minichromosome in the chimpanzee louse.

Conclusions

Using the human pubic louse, Pt. pubis, as an outgroup for comparison, we infer that a single minichromosome has fragmented into three in the lineage leading to the human head louse and the human body louse since this lineage diverged from the chimpanzee louse ~6 million years ago. Our results provide insights into the process of mt genome fragmentation in the sucking lice in a relatively fine evolutionary scale.

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Genomic factors related to tissue tropism in Chlamydia pneumoniae infection

Background

Chlamydia pneumoniae (Cpn) are obligate intracellular bacteria that cause acute infections of the upper and lower respiratory tract and have been implicated in chronic inflammatory diseases. Although of significant clinical relevance, complete genome sequences of only four clinical Cpn strains have been obtained. All of them were isolated from the respiratory tract and shared more than 99% sequence identity. Here we investigate genetic differences on the whole-genome level that are related to Cpn tissue tropism and pathogenicity.

Results

We have sequenced the genomes of 18 clinical isolates from different anatomical sites (e.g. lung, blood, coronary arteries) of diseased patients, and one animal isolate. In total 1,363 SNP loci and 184 InDels have been identified in the genomes of all clinical Cpn isolates. These are distributed throughout the whole chlamydial genome and enriched in highly variable regions. The genomes show clear evidence of recombination in at least one potential region but no phage insertions. The tyrP gene was always encoded as single copy in all vascular isolates. Phylogenetic reconstruction revealed distinct evolutionary lineages containing primarily non-respiratory Cpn isolates. In one of these, clinical isolates from coronary arteries and blood monocytes were closely grouped together. They could be distinguished from all other isolates by characteristic nsSNPs in genes involved in RB to EB transition, inclusion membrane formation, bacterial stress response and metabolism.

Conclusions

This study substantially expands the genomic data of Cpn and elucidates its evolutionary history. The translation of the observed Cpn genetic differences into biological functions and the prediction of novel pathogen-oriented diagnostic strategies have to be further explored.

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Phylogenetic analyses provide the first insights into the evolution of OVATE family proteins in land plants

Background and Aims

The OVATE gene encodes a nuclear-localized regulatory protein belonging to a distinct family of plant-specific proteins known as the OVATE family proteins (OFPs). OVATE was first identified as a key regulator of fruit shape in tomato, with nonsense mutants displaying pear-shaped fruits. However, the role of OFPs in plant development has been poorly characterized.

Methods

Public databases were searched and a total of 265 putative OVATE protein sequences were identified from 13 sequenced plant genomes that represent the major evolutionary lineages of land plants. A phylogenetic analysis was conducted based on the alignment of the conserved OVATE domain from these 13 selected plant genomes. The expression patterns of tomato SlOFP genes were analysed via quantitative real-time PCR. The pattern of OVATE gene duplication resulting in the expansion of the gene family was determined in arabidopsis, rice and tomato.

Key Results

Genes for OFPs were found to be present in all the sampled land plant genomes, including the early-diverged lineages, mosses and lycophytes. Phylogenetic analysis based on the amino acid sequences of the conserved OVATE domain defined 11 sub-groups of OFPs in angiosperms. Different evolutionary mechanisms are proposed for OVATE family evolution, namely conserved evolution and divergent expansion. Characterization of the AtOFP family in arabidopsis, the OsOFP family in rice and the SlOFP family in tomato provided further details regarding the evolutionary framework and revealed a major contribution of tandem and segmental duplications towards expansion of the OVATE gene family.

Conclusions

This first genome-wide survey on OFPs provides new insights into the evolution of the OVATE protein family and establishes a solid base for future functional genomics studies on this important but poorly characterized regulatory protein family in plants.     

A family of small cyclic amphipathic peptides (SCAmpPs) genes in citrus

Background

Citrus represents a crop of global importance both in economic impact and significance to nutrition. Citrus production worldwide is threatened by the disease Huanglongbing (HLB), caused by the phloem-limited pathogen Candidatus Liberibacter spp.. As a source of stable HLB-resistance has yet to be identified, there is considerable interest in characterization of novel disease-associated citrus genes.

Results

A gene family of Small Cyclic Amphipathic Peptides (SCAmpPs) in citrus is described. The citrus genomes contain 100–150 SCAmpPs genes, approximately 50 of which are represented in the citrus EST database. These genes encode small ~50 residue precursor proteins that are post-translationally processed, releasing 5–10 residue cyclic peptides. The structures of the SCAmpPs genes are highly conserved, with the small coding domains interrupted by a single intron and relatively extended untranslated regions. Some family members are very highly transcribed in specific citrus tissues, as determined by representation in tissue-specific cDNA libraries. Comparison of the ESTs of related SCAmpPs revealed an unexpected evolutionary profile, consistent with targeted mutagenesis of the predicted cyclic peptide domain. The SCAmpPs genes are displayed in clusters on the citrus chromosomes, with apparent association with receptor leucine-rich repeat protein arrays. This study focused on three SCAmpPs family members with high constitutive expression in citrus phloem. Unexpectedly high sequence conservation was observed in the promoter region of two phloem-expressed SCAmpPs that encode very distinct predicted cyclic products. The processed cyclic product of one of these phloem SCAmpPs was characterized by LC-MS-MS analysis of phloem tissue, revealing properties consistent with a K⁺ ionophore.

Conclusions

The SCAmpPs amino acid composition, protein structure, expression patterns, evolutionary profile and chromosomal distribution are consistent with designation as ribosomally synthesized defense-related peptides.

Electronic supplementary material

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Anatomical aspects of angiosperm root evolution

Background and Aims

Anatomy had been one of the foundations in our understanding of plant evolutionary trends and, although recent evo-devo concepts are mostly based on molecular genetics, classical structural information remains useful as ever. Of the various plant organs, the roots have been the least studied, primarily because of the difficulty in obtaining materials, particularly from large woody species. Therefore, this review aims to provide an overview of the information that has accumulated on the anatomy of angiosperm roots and to present possible evolutionary trends between representatives of the major angiosperm clades.

Scope

This review covers an overview of the various aspects of the evolutionary origin of the root. The results and discussion focus on angiosperm root anatomy and evolution covering representatives from basal angiosperms, magnoliids, monocots and eudicots. We use information from the literature as well as new data from our own research.

Key Findings

The organization of the root apical meristem (RAM) of Nymphaeales allows for the ground meristem and protoderm to be derived from the same group of initials, similar to those of the monocots, whereas in Amborellales, magnoliids and eudicots, it is their protoderm and lateral rootcap which are derived from the same group of initials. Most members of Nymphaeales are similar to monocots in having ephemeral primary roots and so adventitious roots predominate, whereas Amborellales, Austrobaileyales, magnoliids and eudicots are generally characterized by having primary roots that give rise to a taproot system. Nymphaeales and monocots often have polyarch (heptarch or more) steles, whereas the rest of the basal angiosperms, magnoliids and eudicots usually have diarch to hexarch steles.

Conclusions

Angiosperms exhibit highly varied structural patterns in RAM organization; cortex, epidermis and rootcap origins; and stele patterns. Generally, however, Amborellales, magnoliids and, possibly, Austrobaileyales are more similar to eudicots, and the Nymphaeales are strongly structurally associated with the monocots, especially the Acorales.     

Genomic sequence of the aflatoxigenic filamentous fungus Aspergillus nomius

Background

Aspergillus nomius is an opportunistic pathogen and one of the three most important producers of aflatoxins in section Flavi. This fungus has been reported to contaminate agricultural commodities, but it has also been sampled in non-agricultural areas so the host range is not well known. Having a similar mycotoxin profile as A. parasiticus, isolates of A. nomius are capable of secreting B- and G- aflatoxins.

Results

In this study we discovered that the A. nomius type strain (NRRL 13137) has a genome size of approximately 36 Mb which is comparable to other Aspergilli whose genomes have been sequenced. Its genome encompasses 11,918 predicted genes, 72 % of which were assigned GO terms using BLAST2GO. More than 1,200 of those predicted genes were identified as unique to A. nomius, and the most significantly enriched GO category among the unique genes was oxidoreducatase activity. Phylogenomic inference shows NRRL 13137 as ancestral to the other aflatoxigenic species examined from section Flavi. This strain contains a single mating-type idiomorph designated as MAT1-1.

Conclusions

This study provides a preliminary analysis of the A. nomius genome. Given the recently discovered potential for A. nomius to undergo sexual recombination, and based on our findings, this genome sequence provides an additional evolutionary reference point for studying the genetics and biology of aflatoxin production.     

Functional innovations of three chronological mesohexaploid Brassica rapa genomes

Background

The Brassicaceae family is an exemplary model for studying plant polyploidy. The Brassicaceae knowledge-base includes the well-annotated Arabidopsis thaliana reference sequence; well-established evidence for three rounds of whole genome duplication (WGD); and the conservation of genomic structure, with 24 conserved genomic blocks (GBs). The recently released Brassica rapa draft genome provides an ideal opportunity to update our knowledge of the conserved genomic structures in Brassica, and to study evolutionary innovations of the mesohexaploid plant, B. rapa.

Results

Three chronological B. rapa genomes (recent, young, and old) were reconstructed with sequence divergences, revealing a trace of recursive WGD events. A total of 636 fast evolving genes were unevenly distributed throughout the recent and young genomes. The representative Gene Ontology (GO) terms for these genes were ‘stress response’ and ‘development’ both through a change in protein modification or signaling, rather than by enhancing signal recognition. In retention patterns analysis, 98% of B. rapa genes were retained as collinear gene pairs; 77% of those were singly-retained in recent or young genomes resulting from death of the ancestral copies, while others were multi-retained as long retention genes. GO enrichments indicated that single retention genes mainly function in the interpretation of genetic information, whereas, multi-retention genes were biased toward signal response, especially regarding development and defense. In the recent genome, 13,302, 5,790, and 20 gene pairs were multi-retained following Brassica whole genome triplication (WGT) events with 2, 3, and 4 homoeologous copies, respectively. Enriched GO-slim terms from B. rapa homomoelogues imply that a major effect of the B. rapa WGT may have been to acquire environmental adaptability or to change the course of development. These homoeologues seem to more frequently undergo subfunctionalization with spatial expression patterns compared with other possible events including nonfunctionalization and neofunctionalization.

Conclusion

We refined Brassicaceae GB information using the latest genomic resources, and distinguished three chronologically ordered B. rapa genomes. B. rapa genes were categorized into fast evolving, single- and multi-retention genes, and long retention genes by their substitution rates and retention patterns. Representative functions of the categorized genes were elucidated, providing better understanding of B. rapa evolution and the Brassica genus.

Electronic supplementary material

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Comparative analysis of plant carbohydrate active enZymes and their role in xylogenesis

Background

Carbohydrate metabolism is a key feature of vascular plant architecture, and is of particular importance in large woody species, where lignocellulosic biomass is responsible for bearing the bulk of the stem and crown. Since Carbohydrate Active enZymes (CAZymes) in plants are responsible for the synthesis, modification and degradation of carbohydrate biopolymers, the differences in gene copy number and regulation between woody and herbaceous species have been highlighted previously. There are still many unanswered questions about the role of CAZymes in land plant evolution and the formation of wood, a strong carbohydrate sink.

Results

Here, twenty-two publically available plant genomes were used to characterize the frequency, diversity and complexity of CAZymes in plants. We find that a conserved suite of CAZymes is a feature of land plant evolution, with similar diversity and complexity regardless of growth habit and form. In addition, we compared the diversity and levels of CAZyme gene expression during wood formation in trees using mRNA-seq data from two distantly related angiosperm tree species Eucalyptus grandis and Populus trichocarpa, highlighting the major CAZyme classes involved in xylogenesis and lignocellulosic biomass production.

Conclusions

CAZyme domain ratio across embryophytes is maintained, and the diversity of CAZyme domains is similar in all land plants, regardless of woody habit. The stoichiometric conservation of gene expression in woody and non-woody tissues of Eucalyptus and Populus are indicative of gene balance preservation.

Electronic supplementary material

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Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus

Background

Root-colonizing fluorescent pseudomonads are known for their excellent abilities to protect plants against soil-borne fungal pathogens. Some of these bacteria produce an insecticidal toxin (Fit) suggesting that they may exploit insect hosts as a secondary niche. However, the ecological relevance of insect toxicity and the mechanisms driving the evolution of toxin production remain puzzling.

Results

Screening a large collection of plant-associated pseudomonads for insecticidal activity and presence of the Fit toxin revealed that Fit is highly indicative of insecticidal activity and predicts that Pseudomonas protegens and P. chlororaphis are exclusive Fit producers. A comparative evolutionary analysis of Fit toxin-producing Pseudomonas including the insect-pathogenic bacteria Photorhabdus and Xenorhadus, which produce the Fit related Mcf toxin, showed that fit genes are part of a dynamic genomic region with substantial presence/absence polymorphism and local variation in GC base composition. The patchy distribution and phylogenetic incongruence of fit genes indicate that the Fit cluster evolved via horizontal transfer, followed by functional integration of vertically transmitted genes, generating a unique Pseudomonas-specific insect toxin cluster.

Conclusions

Our findings suggest that multiple independent evolutionary events led to formation of at least three versions of the Mcf/Fit toxin highlighting the dynamic nature of insect toxin evolution.

Electronic supplementary material

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Population structure of mitochondrial genomes in Saccharomyces cerevisiae

Background

Rigorous study of mitochondrial functions and cell biology in the budding yeast, Saccharomyces cerevisiae has advanced our understanding of mitochondrial genetics. This yeast is now a powerful model for population genetics, owing to large genetic diversity and highly structured populations among wild isolates. Comparative mitochondrial genomic analyses between yeast species have revealed broad evolutionary changes in genome organization and architecture. A fine-scale view of recent evolutionary changes within S. cerevisiae has not been possible due to low numbers of complete mitochondrial sequences.

Results

To address challenges of sequencing AT-rich and repetitive mitochondrial DNAs (mtDNAs), we sequenced two divergent S. cerevisiae mtDNAs using a single-molecule sequencing platform (PacBio RS). Using de novo assemblies, we generated highly accurate complete mtDNA sequences. These mtDNA sequences were compared with 98 additional mtDNA sequences gathered from various published collections. Phylogenies based on mitochondrial coding sequences and intron profiles revealed that intraspecific diversity in mitochondrial genomes generally recapitulated the population structure of nuclear genomes. Analysis of intergenic sequence indicated a recent expansion of mobile elements in certain populations. Additionally, our analyses revealed that certain populations lacked introns previously believed conserved throughout the species, as well as the presence of introns never before reported in S. cerevisiae.

Conclusions

Our results revealed that the extensive variation in S. cerevisiae mtDNAs is often population specific, thus offering a window into the recent evolutionary processes shaping these genomes. In addition, we offer an effective strategy for sequencing these challenging AT-rich mitochondrial genomes for small scale projects.

Electronic supplementary material

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High resolution assembly and characterization of genomes of Canadian isolates of Salmonella Enteritidis

Background

There is a need to characterize genomes of the foodborne pathogen, Salmonella enterica serovar Enteritidis (SE) and identify genetic information that could be ultimately deployed for differentiating strains of the organism, a need that is yet to be addressed mainly because of the high degree of clonality of the organism. In an effort to achieve the first characterization of the genomes of SE of Canadian origin, we carried out massively parallel sequencing of the nucleotide sequence of 11 SE isolates obtained from poultry production environments (n = 9), a clam and a chicken, assembled finished genomes and investigated diversity of the SE genome.

Results

The median genome size was 4,678,683 bp. A total of 4,833 chromosomal genes defined the pan genome of our field SE isolates consisting of 4,600 genes present in all the genomes, i.e., core genome, and 233 genes absent in at least one genome (accessory genome). Genome diversity was demonstrable by the presence of 1,360 loci showing single nucleotide polymorphism (SNP) in the core genome which was used to portray the genetic distances by means of a phylogenetic tree for the SE isolates. The accessory genome consisted mostly of previously identified SE prophage sequences as well as two, apparently full- sized, novel prophages namely a 28 kb sequence provisionally designated as SE-OLF-10058 (3) prophage and a 43 kb sequence provisionally designated as SE-OLF-10012 prophage.

Conclusions

The number of SNPs identified in the relatively large core genome of SE is a reflection of substantial diversity that could be exploited for strain differentiation as shown by the development of an informative phylogenetic tree. Prophage sequences can also be exploited for SE strain differentiation and lineage tracking. This work has laid the ground work for further studies to develop a readily adoptable laboratory test for the subtyping of SE.

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