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Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets.

Wu X, Xu X, Yu Z, Kong X - BMC Res Notes (2009)

Bottom Line: Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets.Comparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes.These features provide useful clues and information for evolutionary analysis of scallop mitogenomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key Laboratory of Marine Bio-resource Sustainable Utilization, Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou 510301, PR China. xywu2007@scsio.ac.cn

ABSTRACT

Background: It can be seen from the available mollusk mitogenomes that the family Pectinidae exhibits the most variation in genome organization. In this study, comparative mitogenomic analyses were performed for three scallops from the subfamily Chlamydinae (Pectinidae), with the goal of characterizing the degree of variability of mitogenome organization and other characteristics among species from the same subfamily and exploring their possible evolution route.

Findings: The complete or nearly complete mtDNA sequences of scallop Mimachlamys nobilis (17,935 bp), Mizuhopecten yessoensis (20,964 bp) and Chlamys farreri (17,035 bp) were determined using long PCR amplification and primer walking sequencing strategy. Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets. Only 21, 16, and 17 tRNA genes were detected in the mitogenomes of M. nobilis, M. yessoensis and C. farreri, respectively. Remarkably, no trnS gene could be identified in any of the three scallops. A newly-detected trnA-like sequence within the mitogenome of M. yessoensis seems to exemplify the functional loss of a tRNA gene, and the duplication of trnD in M. yessoensis raises a fundamental question of whether the retention of the tRNA gene copy of 2-tRNAs is easier than that of 4-tRNAs. Analysis of putative evolutionary pathways of gene rearrangement indicates that transposition of neighboring gene blocks may play an important role in the evolution of mitogenomes in scallops. Parsimonious analysis of the genomic variations implies that the mitogenomes of M. yessoensis and C. farreri are likely to derive independently from a common ancestor that was closely related to M. nobilis.

Conclusion: Comparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes. These features provide useful clues and information for evolutionary analysis of scallop mitogenomes.

No MeSH data available.


Related in: MedlinePlus

The putative evolutionary pathway of mitochondrial genomes for three scallops. The hypothetical pathway with the minimum number of gene duplication, deletion and transposition is illustrated. A putative common ancestor of M. yessoensis and C. farreri is shown as it can be most easily and parsimoniously explained. Putative intermediate gene order between "common ancestral gene order" and "M. yessoensis/C. farreri gene order" is also shown to explain the most parsimoniously possible evolutionary pathway of these two species. Symbols are explained under the figure and gene abbreviations are designated as in the text. Genes with identical order in the lineage are put in black/white boxes.
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Figure 3: The putative evolutionary pathway of mitochondrial genomes for three scallops. The hypothetical pathway with the minimum number of gene duplication, deletion and transposition is illustrated. A putative common ancestor of M. yessoensis and C. farreri is shown as it can be most easily and parsimoniously explained. Putative intermediate gene order between "common ancestral gene order" and "M. yessoensis/C. farreri gene order" is also shown to explain the most parsimoniously possible evolutionary pathway of these two species. Symbols are explained under the figure and gene abbreviations are designated as in the text. Genes with identical order in the lineage are put in black/white boxes.

Mentions: It is often difficult to trace the evolutionary pathway of metazoan mitogenomes due either to the generally low number of reorganization events (e.g., mammals) or drastic reorganizations in some animal lineages (e.g., nematodes, snails and brachiopods etc; see [8,9]), particularly in bivalves [e.g., [10,11]]. Phylogentic analyses for five scallops, using the concatenated amino acid sequences of 12 PCGs, resulted a high supported relationship which can be depicted as (A. irradians, (P. magellanicus, (M. nobilis, (M. yessoensis, C. farreri)))) (see Additional file 11). Based on the inferred phylogeny, a putative evolutionary pathway of gene rearrangement in the three species is assumed, and our preferred scenario of mitogenome evolution is further elaborated in Figure 3. In detail, there are at least three permutations between the mitogenomes of M. nobilis and that of a putative common ancestor of M. yessoensis and C. farreri: transposition of trnM1; transposition of the tRNA gene cluster "TPIL2M2", and loss of trnG and trnV. The tRNA gene cluster "HWY" is assumed to have been present in the putative common ancestor, based on the fact that trnH is just downstream of nad4 in C. farreri. Additionally, the absence of trnW and trnY may be artificial due to the incompletely sequenced downstream region. At least four independent events occurred in the mt gene rearrangement of M. yessoensis in the process of derivation from the putative common ancestor: deletion of the tRNA gene cluster "HWY", transposition of gene block "cox1-trnC-trnA" with rrnS, duplication of trnD and the generation of pseudogene PsA. Only one step is then necessary for the rearrangement of C. farreri from the common ancestor, i.e. the transposition of the large fragment "trnC-trnA-rrnS-nad5" with its neighbor block "nad4L-nad6-trnL1-cob".


Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets.

Wu X, Xu X, Yu Z, Kong X - BMC Res Notes (2009)

The putative evolutionary pathway of mitochondrial genomes for three scallops. The hypothetical pathway with the minimum number of gene duplication, deletion and transposition is illustrated. A putative common ancestor of M. yessoensis and C. farreri is shown as it can be most easily and parsimoniously explained. Putative intermediate gene order between "common ancestral gene order" and "M. yessoensis/C. farreri gene order" is also shown to explain the most parsimoniously possible evolutionary pathway of these two species. Symbols are explained under the figure and gene abbreviations are designated as in the text. Genes with identical order in the lineage are put in black/white boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2683862&req=5

Figure 3: The putative evolutionary pathway of mitochondrial genomes for three scallops. The hypothetical pathway with the minimum number of gene duplication, deletion and transposition is illustrated. A putative common ancestor of M. yessoensis and C. farreri is shown as it can be most easily and parsimoniously explained. Putative intermediate gene order between "common ancestral gene order" and "M. yessoensis/C. farreri gene order" is also shown to explain the most parsimoniously possible evolutionary pathway of these two species. Symbols are explained under the figure and gene abbreviations are designated as in the text. Genes with identical order in the lineage are put in black/white boxes.
Mentions: It is often difficult to trace the evolutionary pathway of metazoan mitogenomes due either to the generally low number of reorganization events (e.g., mammals) or drastic reorganizations in some animal lineages (e.g., nematodes, snails and brachiopods etc; see [8,9]), particularly in bivalves [e.g., [10,11]]. Phylogentic analyses for five scallops, using the concatenated amino acid sequences of 12 PCGs, resulted a high supported relationship which can be depicted as (A. irradians, (P. magellanicus, (M. nobilis, (M. yessoensis, C. farreri)))) (see Additional file 11). Based on the inferred phylogeny, a putative evolutionary pathway of gene rearrangement in the three species is assumed, and our preferred scenario of mitogenome evolution is further elaborated in Figure 3. In detail, there are at least three permutations between the mitogenomes of M. nobilis and that of a putative common ancestor of M. yessoensis and C. farreri: transposition of trnM1; transposition of the tRNA gene cluster "TPIL2M2", and loss of trnG and trnV. The tRNA gene cluster "HWY" is assumed to have been present in the putative common ancestor, based on the fact that trnH is just downstream of nad4 in C. farreri. Additionally, the absence of trnW and trnY may be artificial due to the incompletely sequenced downstream region. At least four independent events occurred in the mt gene rearrangement of M. yessoensis in the process of derivation from the putative common ancestor: deletion of the tRNA gene cluster "HWY", transposition of gene block "cox1-trnC-trnA" with rrnS, duplication of trnD and the generation of pseudogene PsA. Only one step is then necessary for the rearrangement of C. farreri from the common ancestor, i.e. the transposition of the large fragment "trnC-trnA-rrnS-nad5" with its neighbor block "nad4L-nad6-trnL1-cob".

Bottom Line: Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets.Comparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes.These features provide useful clues and information for evolutionary analysis of scallop mitogenomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key Laboratory of Marine Bio-resource Sustainable Utilization, Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou 510301, PR China. xywu2007@scsio.ac.cn

ABSTRACT

Background: It can be seen from the available mollusk mitogenomes that the family Pectinidae exhibits the most variation in genome organization. In this study, comparative mitogenomic analyses were performed for three scallops from the subfamily Chlamydinae (Pectinidae), with the goal of characterizing the degree of variability of mitogenome organization and other characteristics among species from the same subfamily and exploring their possible evolution route.

Findings: The complete or nearly complete mtDNA sequences of scallop Mimachlamys nobilis (17,935 bp), Mizuhopecten yessoensis (20,964 bp) and Chlamys farreri (17,035 bp) were determined using long PCR amplification and primer walking sequencing strategy. Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets. Only 21, 16, and 17 tRNA genes were detected in the mitogenomes of M. nobilis, M. yessoensis and C. farreri, respectively. Remarkably, no trnS gene could be identified in any of the three scallops. A newly-detected trnA-like sequence within the mitogenome of M. yessoensis seems to exemplify the functional loss of a tRNA gene, and the duplication of trnD in M. yessoensis raises a fundamental question of whether the retention of the tRNA gene copy of 2-tRNAs is easier than that of 4-tRNAs. Analysis of putative evolutionary pathways of gene rearrangement indicates that transposition of neighboring gene blocks may play an important role in the evolution of mitogenomes in scallops. Parsimonious analysis of the genomic variations implies that the mitogenomes of M. yessoensis and C. farreri are likely to derive independently from a common ancestor that was closely related to M. nobilis.

Conclusion: Comparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes. These features provide useful clues and information for evolutionary analysis of scallop mitogenomes.

No MeSH data available.


Related in: MedlinePlus