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Complete mitochondrial DNA sequence of oyster Crassostrea hongkongensis-a case of "Tandem duplication-random loss" for genome rearrangement in Crassostrea?

Yu Z, Wei Z, Kong X, Shi W - BMC Genomics (2008)

Bottom Line: Complete mt-sequences can reveal information about gene order and its variation, as well as gene and genome evolution when sequences from multiple phyla are compared.There exists significant codon bias, favoring codons ending in A or T and against those ending with C.The mt-genome and new feature presented here reveal and underline the high level variation of gene order and gene content in Crassostrea and bivalves, inspiring more research to gain understanding to mechanisms underlying gene and genome evolution in bivalves and mollusks.

View Article: PubMed Central - HTML - PubMed

Affiliation: 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. carlzyu@scsio.ac.cn

ABSTRACT

Background: Mitochondrial DNA sequences are extensively used as genetic markers not only for studies of population or ecological genetics, but also for phylogenetic and evolutionary analyses. Complete mt-sequences can reveal information about gene order and its variation, as well as gene and genome evolution when sequences from multiple phyla are compared. Mitochondrial gene order is highly variable among mollusks, with bivalves exhibiting the most variability. Of the 41 complete mt genomes sequenced so far, 12 are from bivalves. We determined, in the current study, the complete mitochondrial DNA sequence of Crassostrea hongkongensis. We present here an analysis of features of its gene content and genome organization in comparison with two other Crassostrea species to assess the variation within bivalves and among main groups of mollusks.

Results: The complete mitochondrial genome of C. hongkongensis was determined using long PCR and a primer walking sequencing strategy with genus-specific primers. The genome is 16,475 bp in length and contains 12 protein-coding genes (the atp8 gene is missing, as in most bivalves), 22 transfer tRNA genes (including a suppressor tRNA gene), and 2 ribosomal RNA genes, all of which appear to be transcribed from the same strand. A striking finding of this study is that a DNA segment containing four tRNA genes (trnk1, trnC, trnQ1 and trnN) and two duplicated or split rRNA gene (rrnL5' and rrnS) are absent from the genome, when compared with that of two other extant Crassostrea species, which is very likely a consequence of loss of a single genomic region present in ancestor of C. hongkongensis. It indicates this region seem to be a "hot spot" of genomic rearrangements over the Crassostrea mt-genomes. The arrangement of protein-coding genes in C. hongkongensis is identical to that of Crassostrea gigas and Crassostrea virginica, but higher amino acid sequence identities are shared between C. hongkongensis and C. gigas than between other pairs. There exists significant codon bias, favoring codons ending in A or T and against those ending with C. Pair analysis of genome rearrangements showed that the rearrangement distance is great between C. gigas-C. hongkongensis and C. virginica, indicating a high degree of rearrangements within Crassostrea. The determination of complete mt-genome of C. hongkongensis has yielded useful insight into features of gene order, variation, and evolution of Crassostrea and bivalve mt-genomes.

Conclusion: The mt-genome of C. hongkongensis shares some similarity with, and interesting differences to, other Crassostrea species and bivalves. The absence of trnC and trnN genes and duplicated or split rRNA genes from the C. hongkongensis genome is a completely novel feature not previously reported in Crassostrea species. The phenomenon is likely due to the loss of a segment that is present in other Crassostrea species and was present in ancestor of C. hongkongensis, thus a case of "tandem duplication-random loss (TDRL)". The mt-genome and new feature presented here reveal and underline the high level variation of gene order and gene content in Crassostrea and bivalves, inspiring more research to gain understanding to mechanisms underlying gene and genome evolution in bivalves and mollusks.

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Related in: MedlinePlus

Pair analysis of mitochondrial genome rearrangements with SPRING (Sorting Permutation by Reversals and block-INterchanGes) in the three Crassostrea species. Star symbol denotes indel genes; dots, solid triangles and squares indicate block-interchange genes during putative genome rearrangements of Crassostrea, respectively. Symbols connected by line denote abutted genes. Double-arrows represent directions and steps in putative procedure of genome rearrangements.
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Figure 3: Pair analysis of mitochondrial genome rearrangements with SPRING (Sorting Permutation by Reversals and block-INterchanGes) in the three Crassostrea species. Star symbol denotes indel genes; dots, solid triangles and squares indicate block-interchange genes during putative genome rearrangements of Crassostrea, respectively. Symbols connected by line denote abutted genes. Double-arrows represent directions and steps in putative procedure of genome rearrangements.

Mentions: Genome rearrangement studies are based on genome-wide analysis of gene orders. The variation of mt gene order occurred in Cassostrea were examined closely through pair analysis of genome rearrangements and direct comparison. It is shown that there are at least five permutations between C. gigas and C. virginica (Fig. 3): indel of trnQ1, trnK and duplicated rrnS; transposition of trnN; transpositions of trnG, trnV andMNR; transpositions of trnK1, trnC, rrnS and MNR; and transpositions of trnD, trnM1, trnM2 and trnS2. However, only one single permutation is inferred between C. gigas and C. hongkongensis, involving the indel of four tRNA genes (trnK1, trnC, trnQ1 and trnN) and two duplicated or split rRNA genes (rrnL5' and rrnS), obviously. With three Cassostrea mtDNA genomes, it was supposed to be able to find ancestral genome scenario. However, the distinct feature (absence of a DNA region) of C. hongkongensis mtDNA genome prevented the analysis of reconstructing rearrangement: only the genes that all genomes involved have in common are considered for analysis, i.e. repetitions or gaps (indels) in genomes are excluded. As gene order of C. hongkongensis and C. gigas would be the same if the indel between them is excluded, pair analysis of genome rearrangements in the three genomes would be actually conducted for two genomes (Fig. 3) and hence no ancestral genome scenario could be found for Cassostrea. Clearly, the rearrangement distance of 5 between C. gigas and C. virginica is a great value within a genus, indicating a high degree of rearrangements. Obviously, the distance between C. hongkongensis and C. gigas would normally be 1, even without analysis.


Complete mitochondrial DNA sequence of oyster Crassostrea hongkongensis-a case of "Tandem duplication-random loss" for genome rearrangement in Crassostrea?

Yu Z, Wei Z, Kong X, Shi W - BMC Genomics (2008)

Pair analysis of mitochondrial genome rearrangements with SPRING (Sorting Permutation by Reversals and block-INterchanGes) in the three Crassostrea species. Star symbol denotes indel genes; dots, solid triangles and squares indicate block-interchange genes during putative genome rearrangements of Crassostrea, respectively. Symbols connected by line denote abutted genes. Double-arrows represent directions and steps in putative procedure of genome rearrangements.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2576254&req=5

Figure 3: Pair analysis of mitochondrial genome rearrangements with SPRING (Sorting Permutation by Reversals and block-INterchanGes) in the three Crassostrea species. Star symbol denotes indel genes; dots, solid triangles and squares indicate block-interchange genes during putative genome rearrangements of Crassostrea, respectively. Symbols connected by line denote abutted genes. Double-arrows represent directions and steps in putative procedure of genome rearrangements.
Mentions: Genome rearrangement studies are based on genome-wide analysis of gene orders. The variation of mt gene order occurred in Cassostrea were examined closely through pair analysis of genome rearrangements and direct comparison. It is shown that there are at least five permutations between C. gigas and C. virginica (Fig. 3): indel of trnQ1, trnK and duplicated rrnS; transposition of trnN; transpositions of trnG, trnV andMNR; transpositions of trnK1, trnC, rrnS and MNR; and transpositions of trnD, trnM1, trnM2 and trnS2. However, only one single permutation is inferred between C. gigas and C. hongkongensis, involving the indel of four tRNA genes (trnK1, trnC, trnQ1 and trnN) and two duplicated or split rRNA genes (rrnL5' and rrnS), obviously. With three Cassostrea mtDNA genomes, it was supposed to be able to find ancestral genome scenario. However, the distinct feature (absence of a DNA region) of C. hongkongensis mtDNA genome prevented the analysis of reconstructing rearrangement: only the genes that all genomes involved have in common are considered for analysis, i.e. repetitions or gaps (indels) in genomes are excluded. As gene order of C. hongkongensis and C. gigas would be the same if the indel between them is excluded, pair analysis of genome rearrangements in the three genomes would be actually conducted for two genomes (Fig. 3) and hence no ancestral genome scenario could be found for Cassostrea. Clearly, the rearrangement distance of 5 between C. gigas and C. virginica is a great value within a genus, indicating a high degree of rearrangements. Obviously, the distance between C. hongkongensis and C. gigas would normally be 1, even without analysis.

Bottom Line: Complete mt-sequences can reveal information about gene order and its variation, as well as gene and genome evolution when sequences from multiple phyla are compared.There exists significant codon bias, favoring codons ending in A or T and against those ending with C.The mt-genome and new feature presented here reveal and underline the high level variation of gene order and gene content in Crassostrea and bivalves, inspiring more research to gain understanding to mechanisms underlying gene and genome evolution in bivalves and mollusks.

View Article: PubMed Central - HTML - PubMed

Affiliation: 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. carlzyu@scsio.ac.cn

ABSTRACT

Background: Mitochondrial DNA sequences are extensively used as genetic markers not only for studies of population or ecological genetics, but also for phylogenetic and evolutionary analyses. Complete mt-sequences can reveal information about gene order and its variation, as well as gene and genome evolution when sequences from multiple phyla are compared. Mitochondrial gene order is highly variable among mollusks, with bivalves exhibiting the most variability. Of the 41 complete mt genomes sequenced so far, 12 are from bivalves. We determined, in the current study, the complete mitochondrial DNA sequence of Crassostrea hongkongensis. We present here an analysis of features of its gene content and genome organization in comparison with two other Crassostrea species to assess the variation within bivalves and among main groups of mollusks.

Results: The complete mitochondrial genome of C. hongkongensis was determined using long PCR and a primer walking sequencing strategy with genus-specific primers. The genome is 16,475 bp in length and contains 12 protein-coding genes (the atp8 gene is missing, as in most bivalves), 22 transfer tRNA genes (including a suppressor tRNA gene), and 2 ribosomal RNA genes, all of which appear to be transcribed from the same strand. A striking finding of this study is that a DNA segment containing four tRNA genes (trnk1, trnC, trnQ1 and trnN) and two duplicated or split rRNA gene (rrnL5' and rrnS) are absent from the genome, when compared with that of two other extant Crassostrea species, which is very likely a consequence of loss of a single genomic region present in ancestor of C. hongkongensis. It indicates this region seem to be a "hot spot" of genomic rearrangements over the Crassostrea mt-genomes. The arrangement of protein-coding genes in C. hongkongensis is identical to that of Crassostrea gigas and Crassostrea virginica, but higher amino acid sequence identities are shared between C. hongkongensis and C. gigas than between other pairs. There exists significant codon bias, favoring codons ending in A or T and against those ending with C. Pair analysis of genome rearrangements showed that the rearrangement distance is great between C. gigas-C. hongkongensis and C. virginica, indicating a high degree of rearrangements within Crassostrea. The determination of complete mt-genome of C. hongkongensis has yielded useful insight into features of gene order, variation, and evolution of Crassostrea and bivalve mt-genomes.

Conclusion: The mt-genome of C. hongkongensis shares some similarity with, and interesting differences to, other Crassostrea species and bivalves. The absence of trnC and trnN genes and duplicated or split rRNA genes from the C. hongkongensis genome is a completely novel feature not previously reported in Crassostrea species. The phenomenon is likely due to the loss of a segment that is present in other Crassostrea species and was present in ancestor of C. hongkongensis, thus a case of "tandem duplication-random loss (TDRL)". The mt-genome and new feature presented here reveal and underline the high level variation of gene order and gene content in Crassostrea and bivalves, inspiring more research to gain understanding to mechanisms underlying gene and genome evolution in bivalves and mollusks.

Show MeSH
Related in: MedlinePlus