Molecular Evolution of Viruses: The Origins of Retrons, Retroelements
and Retroviruses
Yechiel Becker
Department of Molecular Virology, Faculty of Medicine, The Hebrew University of
Jerusalem, Jerusalem 91120, ISRAEL.
e-mail: becker@md.huji.ac.il
The discovery of
retrons in the Archeabacteria Myxococcus xanthus and the
Myxobacterium Stigmatella aurantica by Yee and Inouye in 1981 (1) revealed the presence
of a Reverse Transcriptase gene as part of the retroelement, msDNA (multicopy single
stranded DNA), an unusual extrachromosomal RNA-DNA hybrid molecule. Inouye and
Inouye (2) suggested that retrons evolved by acquiring additional genes such as gag and int
leading to the formation of non-LTR retrotransposons. These findings led Temin (3) to
suggest that the reverse transcriptase gene is more ancient than prokaryotic and eukaryotic
cells. It is possible that the appearance of reverse transcriptase gene marked the end of the
“RNA world” and the start of the “DNA world”. The synthesis of DNA molecules on RNA
templates led to the evolution of DNA genomes in primitive cells containing RNA genomes
during a period of one billion years ago (from –4.5x109 to -3.8x109y when cyanobacteria
appeared).
The reverse transcriptase gene had a role in the evolution of the nuclear DNA of the
ancestral eukaryotic cells by generating DNA copies from cellular RNA molecules
resulting in the reinsertion of the DNA molecules as genes and short interspersed repetitive
elements (SINEs) in the eukaryotic cell genome (4). Endogenous retroelements such as
copia in Drosophila, Ty elements in yeast, are present in eukaryotes and contain two genes,
gag and reverse transcriptase. However, the retrotransposon gypsy in Drosophila evolved
into an infectious retrovirus by acquiring an envelope gene, most probably after
recombination with cellular DNA genome. The “gypsy” retrovirus is the most ancient
infectious retrovirus (5) and the progenitor of the retroviruses.
Endogenous retroviruses were found in the genomic DNA of reptiles, amphibians, and bone
fish (6). During the evolution of mammals, the number of retrotransposons and endogenous
retroelements in the nuclear DNA gradually increased. In the human genome, 8% of the
genomic DNA are endogenous retroviruses and retrotransposons, 1-11 Kbp in length (7).
Comparisons of the reverse transcriptase gene and protein to viral RNA directed RNA
polymerase genes and proteins suggested that the two enzymes evolved from a common
ancestor, possibly a retrotransposable element with gag-like and pol-like genes (8). It is
therefore possible to assume that during evolution the reverse transcriptase gene of retrons
in prokaryotes and eukaryotes led to the evolution of RNA and DNA viruses.
References:
1. Yee T and Inouye M. J. Bacteriol 145, 1257-1265, 1981.
2. Inouye M. and Inouye S., J. Bacteriol 174, 2419-2424, 1992.
3. Temin H. Nature 226, 254-255, 1989
4. Hull R. and Covey S.N., Virus Genes 11,105-118, 1996
5. Kim A., Terzian, C., Santamoria, P. Pelisson A., Prudhomme B. and Buchton, A.
Proc. Natl. Acad. Sci USA 91, 1285-1289, 1994.
6. Herinou E., Martin Y et al., Virology 72, 5955-5966, 1998
7. Craig Venter Y et al. Science 291, 1304-1351, 2001
8. Xiong Y and Eickbusch T.H, EMBO J. 9, 3353-3362, 1990