Review

Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes

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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.

    Author information

    Affiliations

    1. School of Molecular and Biomedical Science, The University of Adelaide, South Australia 5005, Australia.

      • Jeremy N. Timmis
      •  & Chun Y. Huang
    2. CSIRO Plant Industry, GPO Box 1600, Australian Capital Territory 2601, Australia.

      • Michael A. Ayliffe
    3. Institute of Botany III, University of Düsseldorf, Düsseldorf 40225, Germany.

      • William Martin

    Authors

    1. Search for Jeremy N. Timmis in:

    2. Search for Michael A. Ayliffe in:

    3. Search for Chun Y. Huang in:

    4. Search for William Martin in:

    Competing interests

    The authors declare no competing financial interests.

    Corresponding author

    Correspondence to Jeremy N. Timmis.

    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+) of Chlamydomonas 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.