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Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes
Nature Reviews Geneticsvolume 5, pages123–135 (2004)Cite this article
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Key Points
Genome sequences show extensive tracts of mitochondrial and plastid DNA that are integrated in nuclear chromosomes. Evidence indicates that an active process of DNA translocation from organelles to the nucleus has been ongoing since the origin or organelles from free-living prokaryotes.
Movement of DNA from organelles to the nucleus occurs at very high rates. These rates have been measured experimentally for mitochondria in yeast and more recently for plastids using transgenic chloroplast technology in tobacco.
Phylogenetic analyses and genome comparisons show that influx of organellar DNA to the nucleus has had a marked quantitative impact on the gene content of eukaryotic chromosomes.
Translocated genes might be expressed to provide products that are targeted to all parts of the cell; there is no magic homing device that targets the products of transferred genes back to the organelle of their origin.
When a relocated gene becomes expressed as a product that provides a selectable advantage, the original, now duplicate copy (be it mitochondrial, plastid or nuclear) can undergo recombination, mutational decay or deletion.
Complete organelle genomes are cropping up in eukaryotic chromosomes, so why are any genes left in organelles at all? The two competing theories that stand in the foreground of this hotly debated issue (redox regulation and hydrophobicity) are contrasted.
Observations from genomes and from experimental transfers favour the view that bulk DNA from lysed organelles is the vector that is responsible for gene relocation, although in some groups of eukaryotes, RNA intermediates have been suggested to act as vectors as well.
DNA movement between genetic compartments has consequences for strategies of genetic manipulation that aim to sequester transgenes in organelles.
The downpour of organelle DNA into eukaryotic chromosomes is an unavoidable consequence of endosymbiosis. This mechanism of natural variation is unique to eukaryotic cells and was an important force in the genesis of eukaryotic genomes.
The impact of endosymbiotic gene transfer on eukaryotic chromosomes was probably greatest in the early phases of organelle origins, before the protein import machinery of mitochondria and chloroplasts had been invented.
Abstract
Genome sequences reveal that a deluge of DNA from organelles has constantly been bombarding the nucleus since the origin of organelles. Recent experiments have shown that DNA is transferred from organelles to the nucleus at frequencies that were previously unimaginable. Endosymbiotic gene transfer is a ubiquitous, continuing and natural process that pervades nuclear DNA dynamics. This relentless influx of organelle DNA has abolished organelle autonomy and increased nuclear complexity.
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Acknowledgements
We thank M. Limpert for help in preparing the manuscript, the Australian Research Council, the Australian–German Joint Research Cooperation Scheme and the Deutsche Forschungsgemeinschaft for financial support, and D. Leister for valuable discussions and permission to modify published figures. Countless individual report on numts, nupts and eukaryotic genes that were acquired from organelles are available; we apologize to all for having to focus on selected and more recent work.
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Authors and Affiliations
School of Molecular and Biomedical Science, The University of Adelaide, South Australia, 5005, Australia
Jeremy N. Timmis & Chun Y. Huang
CSIRO Plant Industry, GPO Box 1600, Australian Capital Territory, 2601, Australia
Michael A. Ayliffe
Institute of Botany III, University of Düsseldorf, Düsseldorf, 40225, Germany
William Martin
- Jeremy N. Timmis
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Correspondence toJeremy N. Timmis.
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Glossary
- CYANOBACTERIA
The group of pigmented, photosynthetic bacteria that contains the endosymbiont ancestors of chloroplasts.
- α-PROTEOBACTERIA
A subgroup of gram-negative bacteria, often called the purple bacteria, that are thought to be the endosymbiont ancestors of mitochondria.
- DISOMIC
The condition in which there are two sets of similar (homologous) chromosomes, such that there are two alleles for each gene locus. These homologous chromosomes pair at meiosis and their segregation and transmission results in Mendelian inheritance.
- HAPLOID
The condition in which there is only a single chromosome, or set of chromosomes, such that all loci are represented by only a single allele.
- CYTOPLASMIC ORGANELLES
Here, confined to mean mitochondria and plastids.
- PROMISCUOUS DNA
DNA that is present in more than one genetic compartment of the eukaryotic cell.
- ARCHAEBACTERIA
An ancient group of organisms that have ribosomes and cell membranes that distinguish them from eubacteria. They sometimes show environmentally extreme ecology.
- NUMT
An acronym to describe nuclear integrants of mitochondrial DNA.
- INTEGRANT
Here, used to describe nuclear tracts of DNA that resemble plastid DNA or mitochondrial DNA.
- NUPT
An acronym to describe nuclear integrants of plastid DNA.
- TRANSIT PEPTIDE
A peptide sequence, often at the N-terminus of a precursor protein, that directs a gene product to its specific cellular destination.
- MUTATIONAL DECAY
The process that describes the random changes that might occur in a DNA sequence in the absence of selection pressure.
- PROTIST
A single-celled eukaryote.
- PHYLOGENETICS
Reconstruction of the evolutionary relationships between sequences using any of a variety of inference methods.
- PRODUCT SPECIFICITY COROLLARY
The situation in which the product of a gene that is donated by a cytoplasmic organelle to the nucleus is expected to be returned to that organelle.
- EPISOME
A unit of genetic material that is composed of a series of genes that sometimes has an independent existence in a host cell and at other times is integrated into a chromosome of the cell, replicating itself along with the chromosome.
- BIOLISTIC TRANSFORMATION
A commonly used transformation method in which metal beads are coated with gene contructs and shot into cells.
- LEAF EXPLANTS
Small sterile sections of leaf or other plant tissue from which whole plants might sometimes be regenerated.
- UNIPARENTAL INHERITANCE
The mode of inheritance that generally characterizes the genes of cytoplasmic organelles in which only one of the two sexual partners contributes to the offspring.
- TRANSPLASTOME
The condition of a plastid genome after the insertion of non-native genes.
- MT− STRAIN
One of the two mating types (the other is mt+) ofChlamydomonas reinhardtii; one of each is required to form a zygote.
- RNA EDITING
Changes in the RNA sequence after transcription is completed. Examples include modification of C to U or of A to I by deamination, or insertion and/or deletion of particular bases.
- PROMOTER TRAP
A genetic engineering technique that involves randomly inserting into the genome constructs that encode an easily detectable marker, such as GFP, but contain no promoter sequences. Marker expression is only detected when the construct lands near an endogenous genomic promoter.
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Timmis, J., Ayliffe, M., Huang, C.et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes.Nat Rev Genet5, 123–135 (2004). https://doi.org/10.1038/nrg1271
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