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Eukaryotic genome evolution: rearrangement and coevolution of compartmentalized genetic information.

ABSTRACT: The plant cell operates with an integrated, compartmentalized genome consisting of nucleus/cytosol, plastids and mitochondria that, in its entirety, is regulated in time, quantitatively, in multicellular organisms and also in space. This genome, as do genomes of eukaryotes in general, originated in endosymbiotic events, with at least three cells, and was shaped phylogenetically by a massive and highly complex restructuring and intermixing of the genetic potentials of the symbiotic partners and by lateral gene transfer. This was accompanied by fundamental changes in expression signals in the entire system at almost all regulatory levels. The gross genome rearrangements contrast with a highly specific compartmental interplay, which becomes apparent in interspecific nuclear-plastid cybrids or hybrids. Organelle exchanges, even between closely related species, can greatly disturb the intracellular genetic balance ("hybrid bleaching"), which is indicative of compartmental coevolution and is of relevance for speciation processes. The photosynthetic machinery of plastids, which is embedded in that genetic machinery, is an appealing model to probe into genomic and organismic evolution and to develop functional molecular genomics. We have studied the reciprocal Atropa belladonna-Nicotiana tabacum cybrids, which differ markedly in their phenotypes, and found that transcriptional and post-transcriptional processes can contribute to genome/plastome incompatibility. Allopolyploidy can influence this phenomenon by providing an increased, cryptic RNA editing potential and the capacity to maintain the integrity of organelles of different taxonomic origins.

SUBMITTER: Herrmann RG

PROVIDER: S-EPMC1693106 | biostudies-other | 2003 Jan

REPOSITORIES: biostudies-other

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Eukaryotic genome evolution: rearrangement and coevolution of compartmentalized genetic information.

Herrmann Reinhold G RG Maier Rainer M RM Schmitz-Linneweber Christian C

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20030101 1429

The plant cell operates with an integrated, compartmentalized genome consisting of nucleus/cytosol, plastids and mitochondria that, in its entirety, is regulated in time, quantitatively, in multicellular organisms and also in space. This genome, as do genomes of eukaryotes in general, originated in endosymbiotic events, with at least three cells, and was shaped phylogenetically by a massive and highly complex restructuring and intermixing of the genetic potentials of the symbiotic partners and b ...[more]

PMID: 12594919

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Project description:BackgroundModularity is important for evolutionary innovation. The recombination of existing units to form larger complexes with new functionalities spares the need to create novel elements from scratch. In proteins, this principle can be observed at the level of protein domains, functional subunits which are regularly rearranged to acquire new functions.ResultsIn this study we analyse the mechanisms leading to new domain arrangements in five major eukaryotic clades (vertebrates, insects, fungi, monocots and eudicots) at unprecedented depth and breadth. This allows, for the first time, to directly compare rates of rearrangements between different clades and identify both lineage specific and general patterns of evolution in the context of domain rearrangements. We analyse arrangement changes along phylogenetic trees by reconstructing ancestral domain content in combination with feasible single step events, such as fusion or fission. Using this approach we explain up to 70% of all rearrangements by tracing them back to their precursors. We find that rates in general and the ratio between these rates for a given clade in particular, are highly consistent across all clades. In agreement with previous studies, fusions are the most frequent event leading to new domain arrangements. A lineage specific pattern in fungi reveals exceptionally high loss rates compared to other clades, supporting recent studies highlighting the importance of loss for evolutionary innovation. Furthermore, our methodology allows us to link domain emergences at specific nodes in the phylogenetic tree to important functional developments, such as the origin of hair in mammals.ConclusionsOur results demonstrate that domain rearrangements are based on a canonical set of mutational events with rates which lie within a relatively narrow and consistent range. In addition, gained knowledge about these rates provides a basis for advanced domain-based methodologies for phylogenetics and homology analysis which complement current sequence-based methods.

Project description:Despite high pertussis vaccine coverage, reported cases of whooping cough (pertussis) have increased over the last decade in the United States and other developed countries. Although Bordetella pertussis is well known for its limited gene sequence variation, recent advances in long-read sequencing technology have begun to reveal genomic structural heterogeneity among otherwise indistinguishable isolates, even within geographically or temporally defined epidemics. We have compared rearrangements among complete genome assemblies from 257 B. pertussis isolates to examine the potential evolution of the chromosomal structure in a pathogen with minimal gene nucleotide sequence diversity. Discrete changes in gene order were identified that differentiated genomes from vaccine reference strains and clinical isolates of various genotypes, frequently along phylogenetic boundaries defined by single nucleotide polymorphisms. The observed rearrangements were primarily large inversions centered on the replication origin or terminus and flanked by IS481, a mobile genetic element with >240 copies per genome and previously suspected to mediate rearrangements and deletions by homologous recombination. These data illustrate that structural genome evolution in B. pertussis is not limited to reduction but also includes rearrangement. Therefore, although genomes of clinical isolates are structurally diverse, specific changes in gene order are conserved, perhaps due to positive selection, providing novel information for investigating disease resurgence and molecular epidemiology.IMPORTANCE Whooping cough, primarily caused by Bordetella pertussis, has resurged in the United States even though the coverage with pertussis-containing vaccines remains high. The rise in reported cases has included increased disease rates among all vaccinated age groups, provoking questions about the pathogen's evolution. The chromosome of B. pertussis includes a large number of repetitive mobile genetic elements that obstruct genome analysis. However, these mobile elements facilitate large rearrangements that alter the order and orientation of essential protein-encoding genes, which otherwise exhibit little nucleotide sequence diversity. By comparing the complete genome assemblies from 257 isolates, we show that specific rearrangements have been conserved throughout recent evolutionary history, perhaps by eliciting changes in gene expression, which may also provide useful information for molecular epidemiology.

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Dataset Information

Eukaryotic genome evolution: rearrangement and coevolution of compartmentalized genetic information.

Publications

Eukaryotic genome evolution: rearrangement and coevolution of compartmentalized genetic information.

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