Origins of genes: "big bang" or continuous creation?

Keese, Paul; Gibbs, Adrian

doi:10.1073/pnas.89.20.9489

Cited by 233 publications

(253 citation statements)

References 57 publications

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“…The hypothesis of overlapping genes origin suggested by Shintani et al (1999) cannot fully explain these phenomena because it is related to 3Ј-end overlaps only and does not consider 5Ј-overlaps at all. Overprinting as the origin of overlapping genes, as suggested by Keese and Gibbs (1992), may provide a better explanation, …”

Section: Discussionmentioning

confidence: 99%

“…Later, one of the genes lost its original polyadenylation signal, but was able to use a signal that happened to be present on the noncoding strand of the other gene. Keese and Gibbs (1992) suspect that overlapping genes arise as a result of overprinting-a process of generating new genes from preexisting nucleotide sequences. However, both studies were done based on a single pair of eukaryotic overlapping genes.…”

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confidence: 99%

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Mammalian Overlapping Genes: The Comparative Perspective

Veeramachaneni¹,

Makałowski²,

Galdzicki³

et al. 2004

Genome Res.

128

130

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It is believed that 3.2 billion bp of the human genome harbor ∼35,000 protein-coding genes. On average, one could expect one gene per 300,000 nucleotides (nt). Although the distribution of the genes in the human genome is not random,it is rather surprising that a large number of genes overlap in the mammalian genomes. Thousands of overlapping genes were recently identified in the human and mouse genomes. However,the origin and evolution of overlapping genes are still unknown. We identified 1316 pairs of overlapping genes in humans and mice and studied their evolutionary patterns. It appears that these genes do not demonstrate greater than usual conservation. Studies of the gene structure and overlap pattern showed that only a small fraction of analyzed genes preserved exactly the same pattern in both organisms

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Mammalian Overlapping Genes: The Comparative Perspective

Veeramachaneni¹,

Makałowski²,

Galdzicki³

et al. 2004

Genome Res.

128

130

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show abstract

“…Although the steps required to generate a new gene by gene duplication or gene rearrangement have been characterized, less is known about the birth of new genes de novo. One particularly intriguing mechanism of de novo gene birth is via "overprinting," in which a novel overprinting gene is encoded as an alternate ORF within an ancestral "overprinted" gene (1). Overprinting results in two unrelated functional proteins encoded as overlapping ORFs within the same DNA sequence.…”

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confidence: 99%

Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes

Carter

Daugherty

Qi³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

148

149

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Many viruses use overprinting (alternate reading frame utilization) as a means to increase protein diversity in genomes severely constrained by size. However, the evolutionary steps that facilitate the de novo generation of a novel protein within an ancestral ORF have remained poorly characterized. Here, we describe the identification of an overprinting gene, expressed from an Alternate frame of the Large T Open reading frame (ALTO) in the early region of Merkel cell polyomavirus (MCPyV), the causative agent of most Merkel cell carcinomas. ALTO is expressed during, but not required for, replication of the MCPyV genome. Phylogenetic analysis reveals that ALTO is evolutionarily related to the middle T antigen of murine polyomavirus despite almost no sequence similarity. ALTO/MT arose de novo by overprinting of the second exon of T antigen in the common ancestor of a large clade of mammalian polyomaviruses. Taking advantage of the low evolutionary divergence and diverse sampling of polyomaviruses, we propose evolutionary transitions that likely gave birth to this protein. We suggest that two highly constrained regions of the large T antigen ORF provided a start codon and C-terminal hydrophobic motif necessary for cellular localization of ALTO. These two key features, together with stochastic erasure of intervening stop codons, resulted in a unique protein-coding capacity that has been preserved ever since its birth. Our study not only reveals a previously undefined protein encoded by several polyomaviruses including MCPyV, but also provides insight into de novo protein evolution. gene evolution | synonymous substitution | disordered motifs T he birth of new genes has fascinated biologists for decades. Although the steps required to generate a new gene by gene duplication or gene rearrangement have been characterized, less is known about the birth of new genes de novo. One particularly intriguing mechanism of de novo gene birth is via "overprinting," in which a novel overprinting gene is encoded as an alternate ORF within an ancestral "overprinted" gene (1). Overprinting results in two unrelated functional proteins encoded as overlapping ORFs within the same DNA sequence. However, the origins of such a complex evolutionary solution have remained elusive.Viruses appear to be especially adept at this form of evolutionary innovation. This frequent use of overprinting is likely the result of the severe constraints imposed on viral genome size, making gene innovation more likely to occur as overprinting rather than within a noncoding region (2). Due to the numerous examples of overprinting in single-stranded RNA viruses, a great deal of research has focused in particular on this class of viruses (3-6). However, small DNA viruses, such as adenoviruses, papillomaviruses, and polyomaviruses, have a similar requirement to maximize the coding capacity of their genomes. In this study, we have taken advantage of our identification of an overprinting gene born in the ancestor of a large clade of polyomaviruses to investigate the...

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“…Also, availability of whole genome sequences showed that vims genes were often contained totally or partially within another gene, in a different reading frame. This observation led Adrian Gibbs to propose the very novel concept of de novo generation of genes by "overprinting," and methods to analyze which of the two overlapping genes was the novel one (Keese and Gibbs 1992).…”

Section: The Early Periodmentioning

confidence: 99%

Questions and Concepts in Plant Virus Evolution: a Historical Perspective

García‐Arenal

Fraile

2008

Plant Virus Evolution

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The interest in plant virus evolution can be dated to the late 1920s, when it was shown that plant virus populations were genetically heterogeneous, and that their composition changed according to the experimental conditions. Many important ideas were generated prior to the era of molecular virology, such as the role of hostand vector-associated selection in virus evolution, and also that small populations, gene coadaptation and evolutionary trade-offs could limit the efficiency of selection. The analysis of viral genomes in the 1980s and 1990s established the quasispecieslike sU'ucture of then populations and allowed extensive analyses of the relationships among virus strains and species. The concept that virus populations had huge sizes and high rates of adaptive mutations became prevalent in this period, with selection mostly invoked as explaining observed patterns of population structure and evolution. In recent times virus evolution has been coming into line with evolutionary biology, and a more complex scenario has emerged. Population bottlenecks during host colonization, during host-to-host transmission or during host population fluctuations may result in smaller population sizes, and genetic drift has been recognized as an important evolutionary factor. Also, particularities of viral genomes such as low levels of neutrality, inultifunctionality of coding and encoded sequences or strong epistasis could constrain the plasticity of viral genomes and hinder then response to selection. Exploring the complexities of plant virus evolution will continue to be a challenge for the future, particularly as it affects host, vector and ecosystem dynamics.

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Origins of genes: "big bang" or continuous creation?

Cited by 233 publications

References 57 publications

Mammalian Overlapping Genes: The Comparative Perspective

Mammalian Overlapping Genes: The Comparative Perspective

Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes

Questions and Concepts in Plant Virus Evolution: a Historical Perspective

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