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Vol. 10, Issue 9, 1307-1318, September 2000

Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses

Harmit S. Malik,2,4 Steve Henikoff,2,1 and Thomas H. Eickbush3

1 Howard Hughes Medical Institute, 2 Fred Hutchinson Cancer Research Center, Seattle, Washington 98109 USA; 3 Department of Biology, University of Rochester, Rochester, New York 14627 USA

Phylogenetic analyses suggest that long-terminal repeat (LTR) bearing retrotransposable elements can acquire additional open-reading frames that can enable them to mediate infection. Whereas this process is best documented in the origin of the vertebrate retroviruses and their acquisition of an envelope (env) gene, similar independent events may have occurred in insects, nematodes, and plants. The origins of env-like genes are unclear, and are often masked by the antiquity of the original acquisitions and by their rapid rate of evolution. In this report, we present evidence that in three other possible transitions of LTR retrotransposons to retroviruses, an envelope-like gene was acquired from a viral source. First, the gypsy and related LTR retrotransposable elements (the insect errantiviruses) have acquired their envelope-like gene from a class of insect baculoviruses (double-stranded DNA viruses with no RNA stage). Second, the Cer retroviruses in the Caenorhabditis elegans genome acquired their envelope gene from a Phleboviral (single ambisense-stranded RNA viruses) source. Third, the Tas retroviral envelope (Ascaris lumricoides) may have been obtained from Herpesviridae (double-stranded DNA viruses, no RNA stage). These represent the only cases in which the env gene of a retrovirus has been traced back to its original source. This has implications for the evolutionary history of retroviruses as well as for the potential ability of all LTR-retrotransposable elements to become infectious agents.

4 Corresponding author. Present address: 1100 Fairview Avenue, A1-162, Seattle, WA 98109 USA.

10:1307-1318 ©2000 by Cold Spring Harbor Laboratory Press  ISSN 1088-9051/00 $5.00
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