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Evolution of C2H2-zinc finger genes revisited.

Thomas JH, Emerson RO - BMC Evol. Biol. (2009)

Bottom Line: One of the main conclusions from the paper is that there is a dramatic rate of gene duplication and gene loss, including the surprising result that 118 human ZF genes are absent in chimpanzee.This discrepancy appears to result from the fact that the SCAN domain did indeed arise before the KRAB domain but is present only in non-ZF genes until a much later date.In addition, we present evidence that provides a more parsimonious explanation for the large proportion of mammalian KRAB-ZF genes without a SCAN domain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genome Sciences, University of Washington, Seattle, 91895, USA. jht@u.washington.edu

ABSTRACT

Background: A recent study by Tadepally et al. describes the clustering of zinc finger (ZF) genes in the human genome and traces their evolutionary history among several placental mammals with complete or draft genome sequences. One of the main conclusions from the paper is that there is a dramatic rate of gene duplication and gene loss, including the surprising result that 118 human ZF genes are absent in chimpanzee. The authors also present evidence concerning the ancestral order in which the ZF-associated KRAB and SCAN domains were recruited to ZF proteins.

Results: Based on our analysis of two of the largest human ZF gene clusters, we find that nearly all of the human genes have plausible orthologs in chimpanzee. The one exception may be a result of the incomplete sequence coverage in the draft chimpanzee genome. The discrepancy in gene content analysis may result from the authors' dependence on the preliminary NCBI gene prediction set for chimpanzee, which appears to either fail to predict or to mispredict many chimpanzee ZF genes. Similar problems may affect the authors' interpretation of the more divergent dog, mouse, and rat ZF gene complements. In addition, we present evidence that the KRAB domain was recruited to ZF genes before the SCAN domain, rather than the reverse as the authors suggest. This discrepancy appears to result from the fact that the SCAN domain did indeed arise before the KRAB domain but is present only in non-ZF genes until a much later date.

Conclusion: When comparing gene content among species, especially when using draft genome assemblies, dependence on preliminary gene prediction sets can be seriously misleading. In such studies, genic sequences must be identified in a manner that is as independent as possible of prediction sets. In addition, we present evidence that provides a more parsimonious explanation for the large proportion of mammalian KRAB-ZF genes without a SCAN domain.

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For each of four species, the Venn diagram represents the number and overlap of predicted genes encoding ZF-C2H2 (blue), KRAB (yellow), and SCAN (red) domains. Numbers correspond to the number of proteins in each category, e.g. chicken has 25 proteins with both KRAB and ZF-C2H2 domains and 2 proteins with only KRAB domains. SCAN domains are present in the prediction sets of T. rubripes and X. tropicalis, but are not associated with ZF-C2H2 proteins. The KRAB domain is not present in T. rubripes, but is already associated with ZF-C2H2 proteins in X. tropicalis. H. sapiens has broad overlaps in its sets of ZF-C2H2, KRAB and SCAN proteins, a pattern typical of mammals.
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Figure 2: For each of four species, the Venn diagram represents the number and overlap of predicted genes encoding ZF-C2H2 (blue), KRAB (yellow), and SCAN (red) domains. Numbers correspond to the number of proteins in each category, e.g. chicken has 25 proteins with both KRAB and ZF-C2H2 domains and 2 proteins with only KRAB domains. SCAN domains are present in the prediction sets of T. rubripes and X. tropicalis, but are not associated with ZF-C2H2 proteins. The KRAB domain is not present in T. rubripes, but is already associated with ZF-C2H2 proteins in X. tropicalis. H. sapiens has broad overlaps in its sets of ZF-C2H2, KRAB and SCAN proteins, a pattern typical of mammals.

Mentions: In order to assess the evolutionary history of the KRAB and SCAN domains with respect to the ZF gene family, we used HMMer software [6] to search all proteins in the Ensembl prediction sets for Takifugu rubripes, Xenopus tropicalis, Gallus gallus and Homo sapiens. Figure 2 shows the numbers and overlaps of proteins containing these three domains in each species. The SCAN domain is present in each species except for chicken, consistent with previous evidence suggesting that SCAN arose in the ancestor of vertebrates and has been lost in chicken [4,7,8]. In the fish and frog we analyzed, the SCAN domain is present but is not found in proteins that also contain ZF domains. This suggests that the fish, frog and chicken genomes contain no SCAN-ZF genes, although we cannot rule out unpredicted genes with this structure.


Evolution of C2H2-zinc finger genes revisited.

Thomas JH, Emerson RO - BMC Evol. Biol. (2009)

For each of four species, the Venn diagram represents the number and overlap of predicted genes encoding ZF-C2H2 (blue), KRAB (yellow), and SCAN (red) domains. Numbers correspond to the number of proteins in each category, e.g. chicken has 25 proteins with both KRAB and ZF-C2H2 domains and 2 proteins with only KRAB domains. SCAN domains are present in the prediction sets of T. rubripes and X. tropicalis, but are not associated with ZF-C2H2 proteins. The KRAB domain is not present in T. rubripes, but is already associated with ZF-C2H2 proteins in X. tropicalis. H. sapiens has broad overlaps in its sets of ZF-C2H2, KRAB and SCAN proteins, a pattern typical of mammals.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667407&req=5

Figure 2: For each of four species, the Venn diagram represents the number and overlap of predicted genes encoding ZF-C2H2 (blue), KRAB (yellow), and SCAN (red) domains. Numbers correspond to the number of proteins in each category, e.g. chicken has 25 proteins with both KRAB and ZF-C2H2 domains and 2 proteins with only KRAB domains. SCAN domains are present in the prediction sets of T. rubripes and X. tropicalis, but are not associated with ZF-C2H2 proteins. The KRAB domain is not present in T. rubripes, but is already associated with ZF-C2H2 proteins in X. tropicalis. H. sapiens has broad overlaps in its sets of ZF-C2H2, KRAB and SCAN proteins, a pattern typical of mammals.
Mentions: In order to assess the evolutionary history of the KRAB and SCAN domains with respect to the ZF gene family, we used HMMer software [6] to search all proteins in the Ensembl prediction sets for Takifugu rubripes, Xenopus tropicalis, Gallus gallus and Homo sapiens. Figure 2 shows the numbers and overlaps of proteins containing these three domains in each species. The SCAN domain is present in each species except for chicken, consistent with previous evidence suggesting that SCAN arose in the ancestor of vertebrates and has been lost in chicken [4,7,8]. In the fish and frog we analyzed, the SCAN domain is present but is not found in proteins that also contain ZF domains. This suggests that the fish, frog and chicken genomes contain no SCAN-ZF genes, although we cannot rule out unpredicted genes with this structure.

Bottom Line: One of the main conclusions from the paper is that there is a dramatic rate of gene duplication and gene loss, including the surprising result that 118 human ZF genes are absent in chimpanzee.This discrepancy appears to result from the fact that the SCAN domain did indeed arise before the KRAB domain but is present only in non-ZF genes until a much later date.In addition, we present evidence that provides a more parsimonious explanation for the large proportion of mammalian KRAB-ZF genes without a SCAN domain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genome Sciences, University of Washington, Seattle, 91895, USA. jht@u.washington.edu

ABSTRACT

Background: A recent study by Tadepally et al. describes the clustering of zinc finger (ZF) genes in the human genome and traces their evolutionary history among several placental mammals with complete or draft genome sequences. One of the main conclusions from the paper is that there is a dramatic rate of gene duplication and gene loss, including the surprising result that 118 human ZF genes are absent in chimpanzee. The authors also present evidence concerning the ancestral order in which the ZF-associated KRAB and SCAN domains were recruited to ZF proteins.

Results: Based on our analysis of two of the largest human ZF gene clusters, we find that nearly all of the human genes have plausible orthologs in chimpanzee. The one exception may be a result of the incomplete sequence coverage in the draft chimpanzee genome. The discrepancy in gene content analysis may result from the authors' dependence on the preliminary NCBI gene prediction set for chimpanzee, which appears to either fail to predict or to mispredict many chimpanzee ZF genes. Similar problems may affect the authors' interpretation of the more divergent dog, mouse, and rat ZF gene complements. In addition, we present evidence that the KRAB domain was recruited to ZF genes before the SCAN domain, rather than the reverse as the authors suggest. This discrepancy appears to result from the fact that the SCAN domain did indeed arise before the KRAB domain but is present only in non-ZF genes until a much later date.

Conclusion: When comparing gene content among species, especially when using draft genome assemblies, dependence on preliminary gene prediction sets can be seriously misleading. In such studies, genic sequences must be identified in a manner that is as independent as possible of prediction sets. In addition, we present evidence that provides a more parsimonious explanation for the large proportion of mammalian KRAB-ZF genes without a SCAN domain.

Show MeSH
Related in: MedlinePlus