Segmented Genome Viruses and the Evolutionary Potential of Asymmetrical Sex

SEGMENTED GENOME VIRUSES AND THE EVOLUTIONARY POTENTIAL OF ASYMMETRICAL SEX EDWIN D. KILBOURNE* The initial recognition that animal viruses might carry their genes in discrete pieces was based on the demonstration by Burnet [1], and later Hirst and his colleagues [2], that dual infection with related but distinguishable influenza viruses resulted in high frequency recombination explicable only as a kind of chromosomal reassortment. It is difficult now to appreciate the heretical nature of that proposition , but heresy it did remain until biochemical studies of the influenza viral RNA demonstrated clearly that separate RNA molecules were isolable from virions [3, 4] and infected cells [5], and that these pieces were not fragments of larger RNAs but had different and unique sequences [6, 7]. Parallel complementation analysis of ts (temperature-sensitive) mutants has provided firm genetic evidence not only with influenza [8, 9] but with reoviruses [10, 11] ofcomplementation groups equal in number to the number of RNA segments. It is known that five different groups of RNA viruses of animals possess divided or segmented genomes, including such dissimilar prototypes as Drosophila X, Bluetongue, Bunyamwera, and infective pancreatic necrosis viruses which are morphologically and biochemically very different. In preparing for a symposium on animal virus genetics, I found it interesting to search for common principles to identify similarities among these agents, although it seemed to me most probable that these disparate viruses have arrived at their common genetic strategy by parallel or convergent evolution. An overriding consideration in this analysis has been the recognition that, to the extent that we can The author is grateful to Dr. D. H. L. Bishop, Dr. B. N. Fields, Dr. W. K. Joklik, and Dr. B. R. Murphy for sharing prepublication manuscripts which materially facilitated the preparation of this paper. Portions of this study were presented at a symposium on animal virus genetics of the American Society for Microbiology, Miami, May 12, 1980. *Department of Microbiology, Mount Sinai School of Medicine of the City University of New York, 1 Gustave L. Levy Place, New York, New York 10029.© 1981 by The University of Chicago. AU rights reserved 003 1-5982/82/250 1-0254$01 .00 66 I Edwin D. Kilbourne ¦ Potential ofAsymmetrical Sex equate the divided genome with facility in genetic interchange, the segmented genome viruses may have an intrinsic evolutionary and adaptive advantage over other viruses competing within the same ecosystem. These viruses are not limited by mutational frequency for their variation but have available an extended gene pool carried by related viruses with which they can carry out genetic reassortment. Common Features ofthe Morphologically Disparate Segmented Genome Viruses Divided genomes come in all kinds of packages as is schematically shown in figure 1. Orthomyxoviridae, Bunyaviridae, and Arenaviridae are enveloped viruses containing negative single-stranded RNA of nonmessage sense. The Reoviridae and a newly recognized group for which the name "birnavirus" has been proposed [12] are naked icosahedral viruses with double-stranded RNA. With all these viruses, those prototypes that have received adequate study have been shown to carry out primary transcription of virion RNA to mRNA using RNA-dependent RNA transcriptase contained within the virus (table 1). In the case of reoviruses and bunyaviruses, and six ENVELOPED, HELICAL NUCLEOCAPSID Arenaviridae ss RNA (2) Orthomyxoviridae ss RNA (8) Bunyaviridae ss RNA (3) NAKED, ICOSAHEDRAL Reoviridae ds RNA (10-12) birnaviruses ds RNA (2) Fiel.—Structural variety of segmented genome animal viruses. Number of RNA segments for each is shown parenthetically. (Drawings modified from third report of the International Committee on Taxonomy of Viruses [47].) Perspectives in Biology and Medicine ¦ Autumn 1981 | 67 TABLE 1 Replication Strategy of Segmented Genome Animal Viruses GeneReassortPrimary TranscriptionProductsment Reovirus ................ ds RNA(IO) -* (+)mRNA(10)10+ Birnavirus .............. ds RNA(2) -» (+)mRNA (?)3 (?) Influenza virus .......... ss RNA(8) -» (+)mRNA(9)9 + Bunyavirus ............. ss RNA(3) -> (+)mRNA(3)4 + Arenavirus ............. ss RNA(2) -» (+)mRNA (?)3-4-?- ??the eight influenza virus RNAs, each negative strand is transcribed to a single message.1 Although coding assignments of the genes of the arenaviruses and bunyaviruses have not been completed, it appears that one or more of the RNAs must code for more than one polypeptide. Bunyaviruses have three RNA segments and code for four proteins...