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Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes.

Sun XJ, Xu PF, Zhou T, Hu M, Fu CT, Zhang Y, Jin Y, Chen Y, Chen SJ, Huang QH, Liu TX, Chen Z - PLoS ONE (2008)

Bottom Line: A group of maternal SET domain genes, which are implicated in the programming of histone modification states in early development, have been identified and predicted to be responsible for all known sites of SET domain-mediated histone methylation.Furthermore, some genes show specific expression patterns in certain tissues at certain stages, suggesting the involvement of epigenetic mechanisms in the development of these systems.These results provide a global view of zebrafish SET domain histone methyltransferases in evolutionary and developmental dimensions and pave the way for using zebrafish to systematically study the roles of these genes during development.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

ABSTRACT
SET domain-containing proteins represent an evolutionarily conserved family of epigenetic regulators, which are responsible for most histone lysine methylation. Since some of these genes have been revealed to be essential for embryonic development, we propose that the zebrafish, a vertebrate model organism possessing many advantages for developmental studies, can be utilized to study the biological functions of these genes and the related epigenetic mechanisms during early development. To this end, we have performed a genome-wide survey of zebrafish SET domain genes. 58 genes total have been identified. Although gene duplication events give rise to several lineage-specific paralogs, clear reciprocal orthologous relationship reveals high conservation between zebrafish and human SET domain genes. These data were further subject to an evolutionary analysis ranging from yeast to human, leading to the identification of putative clusters of orthologous groups (COGs) of this gene family. By means of whole-mount mRNA in situ hybridization strategy, we have also carried out a developmental expression mapping of these genes. A group of maternal SET domain genes, which are implicated in the programming of histone modification states in early development, have been identified and predicted to be responsible for all known sites of SET domain-mediated histone methylation. Furthermore, some genes show specific expression patterns in certain tissues at certain stages, suggesting the involvement of epigenetic mechanisms in the development of these systems. These results provide a global view of zebrafish SET domain histone methyltransferases in evolutionary and developmental dimensions and pave the way for using zebrafish to systematically study the roles of these genes during development.

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Evolution of human lineage-specific SET domain genes.(A) Phylogenetic tree of human SUV39H1, SUV39H2 proteins and their closest homologs in mouse (Mus musculus, Mm), frog (Xenopus tropicalis, Xt) and zebrafish is constructed based on alignment of the amino acid sequences of their SET domains. Human EHMT1 and EHMT2 proteins were used as an outgroup to root the tree. Bootstrap percentages computed from 1000 replicates are shown along the internal braches. (B) Phylogenetic tree of human PRDM7, PRDM9 proteins and their closest homologs in mouse and zebrafish. Human PRDM11 and zebrafish Prdm11 proteins were used as an outgroup to root the tree. (C) Schematic representation of the possible evolutionary history of vertebrate SUV39H1, SUV39H2, PRDM7 and PRDM9 genes. Three gene duplication events through evolution, which give rise to gene pairs in certain lineages, are shown as short bars along the branches, and the common ancestor is depicted as a filled circle. Genes of certain species and the common ancestor are written in boxes.
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pone-0001499-g003: Evolution of human lineage-specific SET domain genes.(A) Phylogenetic tree of human SUV39H1, SUV39H2 proteins and their closest homologs in mouse (Mus musculus, Mm), frog (Xenopus tropicalis, Xt) and zebrafish is constructed based on alignment of the amino acid sequences of their SET domains. Human EHMT1 and EHMT2 proteins were used as an outgroup to root the tree. Bootstrap percentages computed from 1000 replicates are shown along the internal braches. (B) Phylogenetic tree of human PRDM7, PRDM9 proteins and their closest homologs in mouse and zebrafish. Human PRDM11 and zebrafish Prdm11 proteins were used as an outgroup to root the tree. (C) Schematic representation of the possible evolutionary history of vertebrate SUV39H1, SUV39H2, PRDM7 and PRDM9 genes. Three gene duplication events through evolution, which give rise to gene pairs in certain lineages, are shown as short bars along the branches, and the common ancestor is depicted as a filled circle. Genes of certain species and the common ancestor are written in boxes.

Mentions: The phylogenetic analysis of zebrafish and human SET domain genes reveals 2 pairs of potential human lineage-specific paralogs. 1) While human SUV29H1 gene definitely has a pair of co-orthologs in zebrafish (i.e. suv39h1a (GenBank accession DQ840140) and suv39h1b (GenBank accession DQ840139)) as described above, its closest paralog, the human SUV39H2 gene, appears to lack a zebrafish ortholog (Figure 1A; asterisk). 2) A pair of human genes PRDM7 and PRDM9, located on chromosomal regions 16q24.3 and 5p14, respectively, are corresponding to a single zebrafish gene herein named prdm9 (GenBank accession DQ851831) (Figure 1A; double asterisks). To figure out the origin of these human genes, extensive database searches were performed and the resulting sequences were subject to phylogenetic analyses. Interestingly, the results indicate different evolutionary histories of these 2 pairs of human genes. The SUV39H2 gene is found in tetrapod (e.g. human, mouse and frog) but not in zebrafish (Figure 3A), suggesting that this gene is likely generated by a tetrapod lineage-specific duplication event. In contrast, although human possesses a PRDM7 gene and a PRDM9 gene, other vertebrates ranging from zebrafish to mouse just have a single gene, named PRDM9 herein (Figure 3B), suggesting that this pair of human-specific paralogs are result from a gene duplication event after the divergence of the ancestors of human and mouse. Taken together, these data suggest that two different duplication events gave rise to the human lineage-specific paralogs SUV39H1/SUV39H2 genes and PRDM7/PRDM9 genes (Figure 3C).


Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes.

Sun XJ, Xu PF, Zhou T, Hu M, Fu CT, Zhang Y, Jin Y, Chen Y, Chen SJ, Huang QH, Liu TX, Chen Z - PLoS ONE (2008)

Evolution of human lineage-specific SET domain genes.(A) Phylogenetic tree of human SUV39H1, SUV39H2 proteins and their closest homologs in mouse (Mus musculus, Mm), frog (Xenopus tropicalis, Xt) and zebrafish is constructed based on alignment of the amino acid sequences of their SET domains. Human EHMT1 and EHMT2 proteins were used as an outgroup to root the tree. Bootstrap percentages computed from 1000 replicates are shown along the internal braches. (B) Phylogenetic tree of human PRDM7, PRDM9 proteins and their closest homologs in mouse and zebrafish. Human PRDM11 and zebrafish Prdm11 proteins were used as an outgroup to root the tree. (C) Schematic representation of the possible evolutionary history of vertebrate SUV39H1, SUV39H2, PRDM7 and PRDM9 genes. Three gene duplication events through evolution, which give rise to gene pairs in certain lineages, are shown as short bars along the branches, and the common ancestor is depicted as a filled circle. Genes of certain species and the common ancestor are written in boxes.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2200798&req=5

pone-0001499-g003: Evolution of human lineage-specific SET domain genes.(A) Phylogenetic tree of human SUV39H1, SUV39H2 proteins and their closest homologs in mouse (Mus musculus, Mm), frog (Xenopus tropicalis, Xt) and zebrafish is constructed based on alignment of the amino acid sequences of their SET domains. Human EHMT1 and EHMT2 proteins were used as an outgroup to root the tree. Bootstrap percentages computed from 1000 replicates are shown along the internal braches. (B) Phylogenetic tree of human PRDM7, PRDM9 proteins and their closest homologs in mouse and zebrafish. Human PRDM11 and zebrafish Prdm11 proteins were used as an outgroup to root the tree. (C) Schematic representation of the possible evolutionary history of vertebrate SUV39H1, SUV39H2, PRDM7 and PRDM9 genes. Three gene duplication events through evolution, which give rise to gene pairs in certain lineages, are shown as short bars along the branches, and the common ancestor is depicted as a filled circle. Genes of certain species and the common ancestor are written in boxes.
Mentions: The phylogenetic analysis of zebrafish and human SET domain genes reveals 2 pairs of potential human lineage-specific paralogs. 1) While human SUV29H1 gene definitely has a pair of co-orthologs in zebrafish (i.e. suv39h1a (GenBank accession DQ840140) and suv39h1b (GenBank accession DQ840139)) as described above, its closest paralog, the human SUV39H2 gene, appears to lack a zebrafish ortholog (Figure 1A; asterisk). 2) A pair of human genes PRDM7 and PRDM9, located on chromosomal regions 16q24.3 and 5p14, respectively, are corresponding to a single zebrafish gene herein named prdm9 (GenBank accession DQ851831) (Figure 1A; double asterisks). To figure out the origin of these human genes, extensive database searches were performed and the resulting sequences were subject to phylogenetic analyses. Interestingly, the results indicate different evolutionary histories of these 2 pairs of human genes. The SUV39H2 gene is found in tetrapod (e.g. human, mouse and frog) but not in zebrafish (Figure 3A), suggesting that this gene is likely generated by a tetrapod lineage-specific duplication event. In contrast, although human possesses a PRDM7 gene and a PRDM9 gene, other vertebrates ranging from zebrafish to mouse just have a single gene, named PRDM9 herein (Figure 3B), suggesting that this pair of human-specific paralogs are result from a gene duplication event after the divergence of the ancestors of human and mouse. Taken together, these data suggest that two different duplication events gave rise to the human lineage-specific paralogs SUV39H1/SUV39H2 genes and PRDM7/PRDM9 genes (Figure 3C).

Bottom Line: A group of maternal SET domain genes, which are implicated in the programming of histone modification states in early development, have been identified and predicted to be responsible for all known sites of SET domain-mediated histone methylation.Furthermore, some genes show specific expression patterns in certain tissues at certain stages, suggesting the involvement of epigenetic mechanisms in the development of these systems.These results provide a global view of zebrafish SET domain histone methyltransferases in evolutionary and developmental dimensions and pave the way for using zebrafish to systematically study the roles of these genes during development.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

ABSTRACT
SET domain-containing proteins represent an evolutionarily conserved family of epigenetic regulators, which are responsible for most histone lysine methylation. Since some of these genes have been revealed to be essential for embryonic development, we propose that the zebrafish, a vertebrate model organism possessing many advantages for developmental studies, can be utilized to study the biological functions of these genes and the related epigenetic mechanisms during early development. To this end, we have performed a genome-wide survey of zebrafish SET domain genes. 58 genes total have been identified. Although gene duplication events give rise to several lineage-specific paralogs, clear reciprocal orthologous relationship reveals high conservation between zebrafish and human SET domain genes. These data were further subject to an evolutionary analysis ranging from yeast to human, leading to the identification of putative clusters of orthologous groups (COGs) of this gene family. By means of whole-mount mRNA in situ hybridization strategy, we have also carried out a developmental expression mapping of these genes. A group of maternal SET domain genes, which are implicated in the programming of histone modification states in early development, have been identified and predicted to be responsible for all known sites of SET domain-mediated histone methylation. Furthermore, some genes show specific expression patterns in certain tissues at certain stages, suggesting the involvement of epigenetic mechanisms in the development of these systems. These results provide a global view of zebrafish SET domain histone methyltransferases in evolutionary and developmental dimensions and pave the way for using zebrafish to systematically study the roles of these genes during development.

Show MeSH