Recombination also occurs between genes residing on the same piece of nucleic acid Fig. Genes that generally segregate together are called linked genes. If recombination occurs between them, the linkage is said to be incomplete. Recombination of incompletely linked genes occurs in all DNA viruses that have been studied and in several RNA viruses. Recombination by break-rejoin of incompletely linked genes.
The genetic interaction of DNA viruses can result in break-rejoin recombination, in which the two DNA molecules of different viruses break and then cross over. Break-rejoin recombination results more In DNA viruses, as in prokaryotic and eukaryotic cells, recombination between incompletely linked genes occurs by means of a break-rejoin mechanism.
This mechanism involves the actual severing of the covalent bonds linking the bases of each of the two DNA strands in a DNA molecule Fig. Recombination rates for herpesviruses, which are DNA viruses that replicate in the nucleus of infected cells, approximate those expected for a eukaryotic genome of the size of the herpesvirus genome.
Herpesviruses have an average recombination frequency of 10 to 20 percent for any two loci. However, the rate of recombination between a specific pair of genetic loci depends on the distance between them and varies from less than 1 percent to approximately 50 percent. Measurement of the recombination frequencies for different loci can be used to map the virus genome. In this type of genetic map, loci with high recombination frequencies are far apart and loci with low recombination frequencies are close together.
Recombination has been shown to occur in several positive-sense single-stranded RNA virus groups: retroviruses, picornaviruses, and coronaviruses. That is initially surprising, as recombination between RNA molecules has not been observed in prokaryotic or eukaryotic cells. In retroviruses, recombination actually occurs at the point in replication when the retrovirus genome is in a DNA form and takes place by the same break-rejoin mechanism as in cells and DNA viruses.
Recombination between two retroviruses gives rise to novel viral progeny with reassorted genes. Recombination between retroviruses and the host cell can give rise to novel viral progeny that carry nonviral genes.
If these host genes code for growth factors, growth factor receptors, or a number of other specific cellular proteins, the recombinant retroviruses may be oncogenic see Ch. In picornaviruses and coronaviruses, recombination takes place at the level of the interaction of the viral RNA genomes and is not believed to occur by a break-rejoin mechanism. The mechanism is currently believed to be a copy-choice mechanism Fig. Such a weak interaction of the polymerase with the template RNA would permit the polymerase, carrying its RNA strand, to disassociate from the original template nucleic acid strand and then associate with a new template RNA strand.
Recombination frequencies in the range of 0. Therefore, the efficiency of this mechanism of recombination is low. Recombination by copy-choice of incompletely linked genes. The genetic interaction of certain RNA viruses can result in copy-choice recombination. In this mechanism, the polymerase begins replicating RNA template. By an unknown mechanism, which may involve more For example, the novel progeny viruses may have new surface proteins that permit them to infect previously resistant individuals; they may have altered virulence characteristics; they may have novel combinations of proteins that make them infective to new cells in the original host or to new hosts; or they may carry material of cellular origin that gives them oncogenic potential.
Recombination is being used experimentally by virologists to create new vaccines. Vaccinia virus, a DNA virus of the poxvirus group, was used as a live vaccine in the eradication of smallpox. For example, vaccinia virus strains carrying DNA coding for bacterial and viral antigens have been produced.
It is expected that after vaccination with the recombinant vaccinia virus, the bacterial or viral antigen immunogen will be produced. The presence of this immunogen will then stimulate specific antibody production by the host, resulting in protection of the host from the immunogen. Studies with these live, recombinant vaccinia viruses are currently under way to determine whether inoculation of the skin with the recombinant virus can induce a protective host antibody response to the bacterial or viral antigens.
Other studies are investigating the use of live, recombinant adenoviruses containing bacterial or viral genes to infect the gastrointestinal tract and induce both mucosal and systemic immunity.
Development of recombinant vaccinia virus for immunization against cholera toxin. Vaccinia virus genomic DNA is cut with an endonuclease.
A specific sequence of DNA with appropriate regulatory sequences coding for a protein e. In a similar manner, recombinant viruses are also being developed that carry normal human genes. It is envisioned that such recombinant viruses could be useful for gene therapy. Target diseases for gene therapy span a wide range, including diabetes, cystic fibrosis, severe combined immunodeficiency syndrome, etc.
Indeed, treatment of cystic fibrosis patients with replication deficient, recombinant adenoviruses bearing a normal copy of the cystic fibrosis transmembrane regulator gene has already been approved. If these studies give positive results, such directed generation of recombinant viruses may become an important tool in the development of vaccines and for gene therapy. Turn recording back on. National Center for Biotechnology Information , U. Show details Baron S, editor.
Search term. Chapter 43 Viral Genetics W. Robert Fleischmann, Jr. General Concepts Genetic Change in Viruses Viruses are continuously changing as a result of genetic selection. Mutations Mutation Rates and Outcomes The mutation rates of DNA viruses approximate those of eukaryotic cells, yielding in theory one mutant virus in several hundred to many thousand genome copies.
Phenotypic Variation by Mutations Mutations can produce viruses with new antigenic determinants. Vaccine Strains from Mutations Mutations can produce viruses with a reduced pathogenicity, altered host range, or altered target cell specificity but with intact antigenicity.
Recombination Recombination involves the exchange of genetic material between two related viruses during coinfection of a host cell. Recombination by Independent Assortment Recombination by independent assortment can occur among viruses with segmented genomes. Recombination of Incompletely Linked Genes Genes that reside on the same piece of nucleic acid may undergo recombination.
Phenotypic Variation from Recombination Development of viruses with new antigenic determinants by either type of recombination may allow viruses to infect and cause disease in previously immune hosts. Vaccines through Recombination Vaccine strains of viruses can be used to create recombinant viruses that carry extra genes coding for a specific immunogen. Introduction Viruses are simple entities, lacking an energy-generating system and having very limited biosynthetic capabilities.
Genetic Change in Viruses This chapter covers the mechanisms by which genetic changes occur in viruses. Mutations Mutations arise by one of three mechanisms: 1 by the effects of physical mutagens UV light, x-rays on nucleic acids; 2 by the natural behavior of the bases that make up nucleic acids resonance from keto to enol and from amino to imino forms , and 3 through the fallibility of the enzymes that replicate the nucleic acids.
Mutation Rates and Outcomes DNA viruses have mutation rates similar to those of eukaryotic cells because, like eukaryotic DNA polymerases, their replicatory enzymes have proofreading functions. Phenotypic Variation by Mutations Mutations that alter the viral phenotype but are not deleterious may be important.
Figure Mutation causing phenotypic antigenic variation. Vaccine Strains from Mutations Mutation has been a principal tool of virologists in developing attenuated live virus vaccines Table Table Live Attenuated Virus Vaccines.
Recombination Viral recombination occurs when viruses of two different parent strains coinfect the same host cell and interact during replication to generate virus progeny that have some genes from both parents. Although these viruses, particularly the latter three families, mostly encode highly diverged presumably, fast-evolving protein sequences and are currently represented by only a few genomes each, phylogenomic analysis suggests that they comprise a monophyletic group, with several signature genes that are not found in other viruses Jehle et al.
Polydnaviruses represent a unique group of viruses that are only vertically transmitted, with the virus genomes permanently integrated in the genomes of the insect hosts. Nevertheless, even in this unusual case, phylogenetic analysis of the retained viral genes indicates that polydnaviruses are highly derived descendants of nudiviruses Herniou et al. However, this remains but a tentative clue until a comprehensive study on the evolution of these unusual viruses is performed.
The highly diversified order Herpesvirales is of special interest from the standpoint of virus evolution because of a distinct connection with tailed viruses of the order Caudovirales which includes three families, namely Siphoviridae , Podoviridae and Myoviridae.
Caudovirales are nearly ubiquitous in Bacteria Ackermann and Prangishvili, and are also present in diverse orders of Archaea, including the deeply branching archaeal phylum Thaumarchaeota Krupovic et al. The putative bacterial or archaeal virus ancestors of the herpesviruses are unrelated to the tectiviruses, the likely ancestors of the Polintovirus-related majority of eukaryotic dsDNA viruses Fig.
Herpesviruses share with the Caudovirales homologous major capsid proteins of the HK97 fold that is unrelated to the double jelly-roll fold present in the capsid proteins of numerous groups of icosahedral viruses including the Polintovirus-centered assemblage , terminases packaging ATPases-nucleases , and capsid maturation proteases as well as several other proteins Pietila et al. Thus, tailed prokaryotic viruses and herpesviruses share a complex and unique virion assembly and maturation program which is not found in other dsDNA viruses.
The apparent bacteriophage origin of the herpesvirus morphogenesis module that consists of a capsid protein, an ATPase and a protease is a striking parallel with the similar evolutionary route of the Polintovirus ancestor but the actual proteins involved are unrelated or in the case of the ATPase, distantly related.
This evolutionary parallelism clearly reflects a general trend in the origins of the largest, most complex viruses of eukaryotes. Somewhat ironically, bacteriophages of the order Caudovirales , which are the most common viruses on earth, gave rise to a single even if diverse group of eukaryotic dsDNA viruses, whereas the bulk of eukaryotic dsDNA viruses seem to originate from the narrowly spread tectiviruses. Conceivably, the key event behind the success of the Polintoviruses that defined the wide spread of their descendants was the acquisition of the transposase see above.
Furthermore, the fact that herpesviruses seem to be limited to animal hosts might indicate that this group of viruses emerged relatively late in the course of eukaryotic evolution, with the ancestor bacteriophage coming not from the proto-mitochondrion but from a distinct perhaps transient bacterial symbiont of early animals.
Paradoxically, however, the proto-mitochondrial symbiont apparently did contain a provirus derived from a tailed bacteriophage and this provirus had a significant effect on the evolution of mitochondria: in modern mitochondria, ancestral bacterial genes for RNA polymerase, DNA polymerase and DNA primase have been all replaced with the counterparts from the resident prophage early in eukaryogenesis Filee and Forterre, , Shutt and Gray, Finally, the two families of dsDNA viruses with small, circular genomes, Papillomaviridae and Polyomaviridae , appear to have evolved via a route that is completely distinct from the origins of all larger dsDNA viruses of eukaryotes.
The capsids of papillomaviruses and polyomaviruses are constructed from JRC proteins homologous to those of eukaryotic ssDNA viruses Fig. Furthermore, the single multidomain replicative protein of these viruses, known as the large T antigen in polyomaviruses and the E1 protein in papillomaviruses, is homologous to the replication proteins of ssDNA viruses, such as circoviruses, nanoviruses, parvoviruses and geminiviruses Fig. This large protein has a typical domain architecture consisting of a S3H and a rolling circle replication initiation endonuclease that, however, is inactivated in papillomaviruses and polyomaviruses Fig.
Thus, the small dsDNA viruses of eukaryotes apparently are derivatives of ssDNA viruses which themselves evolved via recombination of bacterial rolling circle-replicating plasmids and ssRNA viruses see above.
Overall, the emerging picture of the origin of dsDNA viruses of eukaryotes reveals three readily identifiable bacterial roots Fig. Two of these lines of descent come from distinct groups of bacteriophages and gave rise to the majority of large eukaryotic viruses, whereas the third one comes from plasmids and yielded the two families of small dsDNA viruses that actually are derivatives of ssDNA viruses.
There is no evidence of a direct contribution of viruses infecting archaea to the emergence of eukaryotic virome, despite the remarkable diversity and abundance of archaeal dsDNA viruses Prangishvili, , Prangishvili et al. Given this demonstrable bacterial ancestry, the reconstruction of the evolution of eukaryotic dsDNA viruses seems to be best compatible with the symbiogenetic scenario of eukaryogenesis.
Acquisition of DNA polymerases and primases from the eukaryotic hosts opened the route of genome expansion to the evolving dsDNA viruses, resulting in acquisition of numerous genes from the hosts and exaptation recruitment of the acquired genes for virus-host interaction. The recent dramatic expansion of the collection of viral genome sequences, combined with the concerted efforts in evolutionary genomics, translates into a new level of understanding of the origins of the major groups of eukaryotic viruses and the key events in their evolution.
We now can delineate both the major general trends in the evolution of eukaryotic viruses and specific scenarios for different virus classes. One of the most striking trends is the distinct composition of the eukaryotic virome compared to the viromes of archaea and bacteria, namely, the high prevalence and enormous diversity of RNA viruses. It might be tempting to directly derive the eukaryotic RNA virome from the hypothetical primordial RNA world but the plausibility of this link depends on the adopted scenario for the origin of eukaryotes.
The primordial origin of eukaryotic RNA viruses appears to be compatible with the protoeukaryotic but not with the symbiogenetic scenario. If, under the latter scenario, the host of the mitochondrial endosymbiont was a typical archaeon, the existence of a diverse RNA virome in such an organism appears exceedingly unlikely. Instead, a more circuitous path to the eukaryotic RNA virome would have to be postulated, with traceable contributions from bacterial retroelements as well as bona fide bacterial genes.
This type of chimeric origin is a pervasive theme in the evolution of all classes of eukaryotic viruses that is particularly apparent in the emerging histories of dsRNA viruses, ssDNA viruses and dsDNA viruses. Strikingly, in each of these cases, the morphogenetic and replication-expression modules appear to be of different evolutionary provenances, and recombination between these distinct modules gave rise to a novel type of viruses. At least in some cases, the recombination of modules and spread of individual genes, such as the movement protein gene in plants, seems to have a clear adaptive value by opening up a major new niche for viruses with different particular replication-expression strategies and virion structures.
Another major trend in the evolution of the viruses of eukaryotes is the pervasive evolutionary connection between bona fide viruses and non-viral mobile genetic elements, such as transposons and plasmids. These non-viral elements appear to have made major contributions to the evolution of all classes of eukaryotic viruses as well as the hosts. Furthermore, elements with a dual life style, such as metaviruses and pseudoviruses as well as polintoviruses polintons , appear to have played central roles in the evolution of the retroviruses and large dsDNA viruses of eukaryotes, respectively.
Perhaps, the most remarkable aspect of the evolution of the viruses of eukaryotes is that it seems to be tractable, at least in its central features. The authors thank David Karlin and Tero Ahola for the kind permission to cite the results of their work before publication.
Appendix A Supplementary data associated with this article can be found in the online version at doi National Center for Biotechnology Information , U. Published online Mar Eugene V.
Dolja , b and Mart Krupovic c. Valerian V. Author information Article notes Copyright and License information Disclaimer. Koonin: vog. Dolja: ude. Copyright notice. Elsevier hereby grants permission to make all its COVIDrelated research that is available on the COVID resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source.
This article has been cited by other articles in PMC. Associated Data Supplementary Materials Supplementary material. Abstract Viruses and other selfish genetic elements are dominant entities in the biosphere, with respect to both physical abundance and genetic diversity. Keywords: Evolution of viruses, Transposable elements, Polintons, Bacteriophages, Recombination, Functional gene modules.
Introduction A major discovery of environmental genomics over the last decade is that the most common and abundant biological entities on earth are viruses, in particular bacteriophages Edwards and Rohwer, , Rohwer, , Rohwer and Thurber, , Suttle, , Suttle, The contrasting viromes of prokaryotes and eukaryotes The high level classification of viruses that was introduced by Baltimore in largely inspired by his co-discovery, with Temin, of reverse transcription in animal tumor viruses is based on the replication-expression strategies and in particular on the form of nucleic acid that is incorporated into virions obviously, this criterion is only applicable to bona fide viruses Baltimore, Open in a separate window.
Evolutionary scenarios for the origin of eukaryotes and their impact on the reconstruction of virus evolution The origin of eukaryotes is a major problem in evolutionary biology that is generally considered to be unresolved. Origins of the major classes of eukaryotic viruses and evolutionary relationships between viruses of prokaryotes and eukaryotes A general perspective on RNA virus evolution: Out of the primordial RNA world? Negative-strand RNA viruses: The emerging positive-strand connection Negative-strand RNA viruses of eukaryotes include the order Mononegavirales that consists of three related virus families with non-segmented genomes and 5 families of viruses with segmented genomes Supplementary Table S3.
Synopsis on eukaryotic RNA virome To recapitulate the key points on the eukaryotic RNA virome, the enormous diversity of RNA viruses is a hallmark of the eukaryotic part of the virus world.
Retroelements and retroviruses: Viruses as derived forms An extremely common and abundant class of selfish elements in eukaryotes consists of reverse-transcribing elements or retroelements for short , including retroviruses. Synopsis on eukaryotic retroelements To summarize, the retroelements enjoyed no less success in eukaryotes than RNA viruses with which they could share the ultimate common origin from prokaryotic Group II elements self-splicing introns.
Origins of ssDNA viruses of eukaryotes: Multiple crosses between plasmids and RNA viruses Viruses with ssDNA genomes are increasingly appreciated as a rapidly expanding, highly diverse class of economically, medically and ecologically important pathogens. Origins and primary diversification of eukaryotic dsDNA viruses: The bacteriophage and transposable element connections Compared to RNA viruses and retroelements, dsDNA viruses and mobile elements are somewhat less diverse and less abundant in eukaryotes but nevertheless have been identified in all major eukaryotic groups.
Synopsis of dsDNA virus evolution Overall, the emerging picture of the origin of dsDNA viruses of eukaryotes reveals three readily identifiable bacterial roots Fig.
Conclusions The recent dramatic expansion of the collection of viral genome sequences, combined with the concerted efforts in evolutionary genomics, translates into a new level of understanding of the origins of the major groups of eukaryotic viruses and the key events in their evolution. Acknowledgments The authors thank David Karlin and Tero Ahola for the kind permission to cite the results of their work before publication.
Footnotes Appendix A Supplementary data associated with this article can be found in the online version at doi Appendix A. Supplementary materials Supplementary material Click here to view.
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Viruses and other selfish genetic elements are dominant entities in the biosphere, with respect to both physical abundance and genetic diversity. Various selfish elements parasitize on all cellular life forms. The relative abundances of different classes of viruses are dramatically different between prokaryotes and eukaryotes. In prokaryotes, the great majority of viruses possess double-stranded ds DNA genomes, with a substantial minority of single-stranded ss DNA viruses and only limited presence of RNA viruses.
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