Dynamic Evolution of Eukaryotic Mitochondrial and Nuclear Genomes: A Case Study in the Gourmet Pine Mushroom Tricholoma matsutake

Fungi, as eukaryotic organisms, contain two genomes, the mitochondrial genome and the nuclear genome, in their cells. How the two genomes evolve and correlate to each other is debated. Herein, taking the gourmet pine mushroom Tricholoma matsutake as an example, we performed comparative mitogenomic analysis using samples collected from diverse locations and compared the evolution of the two genomes. The T. matsutake mitogenome encodes 49 genes and is rich of repetitive and non-coding DNAs. Six genes were invaded by up to 11 group I introns, with one cox1 intron cox1P372 showing presence/absence dynamics among different samples. Bioinformatic analyses suggested limited or no evidence of mitochondrial heteroplasmy. Interestingly, hundreds of mitochondrial DNA fragments were found in the nuclear genome, with several larger than 500 nt confirmed by PCR assays and read count comparisons, indicating clear evidence of transfer of mitochondrial DNA into the nuclear genome. Nuclear DNA of T. matsutake showed a higher mutation rate than mitochondrial DNA. Furthermore, we found evidence of incongruence between phylogenetic trees derived from mitogenome and nuclear DNA sequences. Together, our results reveal the dynamic genome evolution of the gourmet pine mushroom.Peer reviewe

The complete mitogenome of two Australian lampreys: mordacia mordax and mordacia praecox

As one of only two surviving outgroups to all jawed vertebrates, lampreys (Petromyzontiformes) can provide important information in our understanding of early vertebrate evolution. However, with many phylogenetic aspects of lamprey evolution still uncertain, the ability to use contemporary lampreys in this role depends on robust phylogenetic hypotheses regarding the interrelationship of the three lamprey families, as well as the relationship between lampreys and hagfishes. To achieve this, complete mitogenome data of Southern Hemisphere lampreys is required. Another contentious issue in lamprey taxonomy is the status of paired species. Whilst many studies have focused on Northern Hemisphere species pairs, this study is the first to compare Mordacia mordax and Mordacia praecox, two lamprey species endemic to Australia and the only species pair in the Southern Hemisphere. The complete mitochondrial genome of Mordacia mordax and Mordacia praecox was determined twice independently, in a single shotgun sequencing run on an Ion Torrent PGM, and using a combination of Sanger sequencing of short range PCR products and Roche 454 GS Junior pyrosequencing of long range PCR products. Both of the mitogenomes contain the 37 typical vertebrate genes. Their gene order and contents are identical to those of previously described lamprey mitogenomes, with the exception of a novel tandem repeat array located between Cyt b and tRNA proline. The tandem repeat array, referred to as NCIII, contains pseudogenes of tRNA proline and phenylalanine, indicating that it has arisen by tandem duplication of the tRNA proline – phenylalanine region. Characterisation of NCIII revealed that the number of repeat copies was polymorphic between individuals of both species, and was a source of both intra-individual and inter-individual variation. Consistent with other studies of lamprey species pairs, the mitogenome of M. mordax and M. praecox are nearly identical. Phylogenetic analyses were carried out using the newly determined mitogenomes, together with five additional lamprey species and two hagfishes. Most tree topologies obtained strongly support the hypothesis that Petromyzontidae plus Geotriidae are a clade whose sister group is Mordaciidae. Additionally, lamprey divergence times were estimated by a temporally-calibrated phylogenetic analysis that included 20 vertebrate mitogenomes and was done using nine well-established fossil calibration points. The recovered topology strongly supported the hypothesis that lampreys separated from hagfishes about 409 MYA, and that lamprey divergence involved the early radiation of Mordaciidae (about 132 MYA), followed by the monophyletic divergence of Geotriidae plus Petromyzontidae about 85 MYA. Taken together, the results in this study provide robust hypotheses regarding the interrelationship of lamprey families and the relationship between hagfish and lampreys, whilst providing an estimation of their divergence times

Genome Evolution in the Salicaceae: Genetic Novelty, Horizontal Gene Transfer, and Comparative Genomics

Genome evolution is a powerful force which shapes genomes over time through processes like mutation, horizontal transfer, and sexual reproduction. Although questions which aim to explore genome evolution are broad, they are all understood through the discovery and comparison of genetic variation. For example, genetic diversity may explain differences in phenotypes, etiology of disease, and is essential for phylogenomic analysis. Recently, the democratization of next generation and third generation DNA sequencing technologies have allowed for genomics to produce large amounts of sequence data. This has facilitated the capture of genetic variation at species and population scales. Populus and Salix are members of the Salicaceae family and are ecologically and economically important woody plants. Currently, there are multiple high-quality reference genomes available for these two genera. Two important sources of genome evolution that will be explored here are genetic novelty in the form of new genes and horizontal gene transfer from the organelle genomes. In the context of genome evolution, both processes have been shown to contribute to beneficial phenotypes as well as disease. The primary contributions of this dissertation research are to identify and assign putative functions to orphan and de novo genes in P. trichocarpa, identify and compare horizontal transfer from the organelle genomes to the nuclear genomes of P. trichocarpa and P. deltoides, and generate new organelle genome resources for 6 different Salix species

Organelle Genetics in Plants

Chloroplasts in photosynthetic organisms and mitochondria in a vast majority of eukaryotes, contain part of the genetic material of a eukaryotic cell. The organisation and inheritance patterns of this organellar DNA are quite different to that of nuclear DNA. Present-day chloroplast and mitochondrial genomes contain only a few dozen genes. Nevertheless, these organelles harbor several thousand proteins, the vast majority of them encoded by the nucleus. As a result, the expression of nuclear and organelle genomes has to be very precisely coordinated. The selection of experimental and review papers of this book covers a wide range of topics related to chloroplasts and plant mitochondria research, illustrating recent advances and diverse insights into the field of organelle genetics in plants. These works represent some of the latest research on the genetics, genomics, and biotechnology of plant mitochondria and chloroplasts, and they are of significant broad interest for the community of plant scientists, especially for those working in the subjects related to organelle genetic

Complete vertebrate mitogenomes reveal widespread repeats and gene duplications

Abstract: Background: Modern sequencing technologies should make the assembly of the relatively small mitochondrial genomes an easy undertaking. However, few tools exist that address mitochondrial assembly directly. Results: As part of the Vertebrate Genomes Project (VGP) we develop mitoVGP, a fully automated pipeline for similarity-based identification of mitochondrial reads and de novo assembly of mitochondrial genomes that incorporates both long (> 10 kbp, PacBio or Nanopore) and short (100–300 bp, Illumina) reads. Our pipeline leads to successful complete mitogenome assemblies of 100 vertebrate species of the VGP. We observe that tissue type and library size selection have considerable impact on mitogenome sequencing and assembly. Comparing our assemblies to purportedly complete reference mitogenomes based on short-read sequencing, we identify errors, missing sequences, and incomplete genes in those references, particularly in repetitive regions. Our assemblies also identify novel gene region duplications. The presence of repeats and duplications in over half of the species herein assembled indicates that their occurrence is a principle of mitochondrial structure rather than an exception, shedding new light on mitochondrial genome evolution and organization. Conclusions: Our results indicate that even in the “simple” case of vertebrate mitogenomes the completeness of many currently available reference sequences can be further improved, and caution should be exercised before claiming the complete assembly of a mitogenome, particularly from short reads alone

Signals of selection in the mitogenome provide insights into adaptation mechanisms in heterogeneous habitats in a widely distributed pelagic fish

Oceans are vast, dynamic, and complex ecosystems characterized by fluctuations in environmental parameters like sea surface temperature (SST), salinity, oxygen availability, and productivity. Environmental variability acts as the driver of organismal evolution and speciation as organisms strive to cope with the challenges. We investigated the evolutionary consequences of heterogeneous environmental conditions on the mitogenome of a widely distributed small pelagic fish of Indian ocean, Indian oil sardine, Sardinella longiceps. Sardines were collected from different eco-regions of the Indian Ocean and selection patterns analyzed in coding and non-coding regions. Signals of diversifying selection were observed in key functional regions involved in OXPHOS indicating OXPHOS gene regulation as the critical factor to meet enhanced energetic demands. A characteristic control region with 38–40 bp tandem repeat units under strong selective pressure as evidenced by sequence conservation and low free energy values was also observed. These changes were prevalent in fishes from the South Eastern Arabian Sea (SEAS) followed by the Northern Arabian Sea (NAS) and rare in Bay of Bengal (BoB) populations. Fishes belonging to SEAS exhibited accelerated substitution rate mainly due to the selective pressures to survive in a highly variable oceanic environment characterized by seasonal hypoxia, variable SST, and food availability