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Exceptionally high cumulative percentage of NUMTs originating from linear mitochondrial DNA molecules in the Hydra magnipapillata genome.

Song S, Jiang F, Yuan J, Guo W, Miao Y - BMC Genomics (2013)

Bottom Line: We found that H. magnipapillata is an exceptional ancestral metazoan with a high NUMT cumulative percentage but a large genome, and its mitochondrial genome linearisation might be responsible for the NUMT enrichment.In addition, NUMT expression analyses showed that NUMTs are co-expressed with adjacent protein-coding genes, suggesting the relevance of their biological function.Taken together, our results provide valuable information for understanding the impact of mitochondrial genome structure on the interaction of mitochondrial molecules and nuclear genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming, Yunnan 650201, China.

ABSTRACT

Background: In contrast to most animal genomes, mitochondrial genomes in species belonging to the phylum Cnidaria show distinct variations in genome structure, including the mtDNA structure (linear or circular) and the presence or absence of introns in protein-coding genes. Therefore, the analysis of nuclear insertions of mitochondrial sequences (NUMTs) in cnidarians allows us to compare the NUMT content in animals with different mitochondrial genome structures.

Results: NUMT identification in the Hydra magnipapillata, Nematostella vectensis and Acropora digitifera genomes showed that the NUMT density in the H. magnipapillata genome clearly exceeds that in other two cnidarians with circular mitochondrial genomes. We found that H. magnipapillata is an exceptional ancestral metazoan with a high NUMT cumulative percentage but a large genome, and its mitochondrial genome linearisation might be responsible for the NUMT enrichment. We also detected the co-transposition of exonic and intronic fragments within NUMTs in N. vectensis and provided direct evidence that mitochondrial sequences can be transposed into the nuclear genome through DNA-mediated fragment transfer. In addition, NUMT expression analyses showed that NUMTs are co-expressed with adjacent protein-coding genes, suggesting the relevance of their biological function.

Conclusions: Taken together, our results provide valuable information for understanding the impact of mitochondrial genome structure on the interaction of mitochondrial molecules and nuclear genomes.

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NUMT lengths distribution.
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Figure 2: NUMT lengths distribution.

Mentions: We determined the homology relationships between the three cnidarian nuclear genomes and their corresponding mitochondrial genomes using BLASTN searches. A total of 704, 24 and 1 NUMTs were inferred in Hydra magnipapillata, Nematostella vectensis, and Acropora digitifera, respectively (Figure 1, Additional file 1: Table S1, Table S2, Additional file 2: Table S3, and Additional file 3: Table S4). The length distribution of the BLASTN hits was 51 to 7,684 bp (mean: 753 bp) for H. magnipapillata, 76 to 1,836 bp (mean: 768 bp) for N. vectensis, and 86 bp for A. digitifera (Figure 2). No obvious differences were observed in the length of NUMTs between H. magnipapillata and N. vectensis (mean lengths: 753 bp and 768 bp, respectively; Student’s t test: P = 0.8536), while their mean lengths were much longer than those observed in many other metazoans (e.g., Amphimedon queenslandica: 222 bp; Drosophila sechellia: 240 bp; Homo sapiens: 309 bp; Nasonia vitripenni: 565 bp) [5,35]. The largest proportion of NUMTs was between 100 and 200 bp in H. magnipapillata and between 800 and 900 bp in N. vectensis (Figure 2). The sequence similarity detected using BLASTN between NUMTs and homologous mtDNA sequences was 79.34 to 100%, 92.11 to 100%, and 95.35% in H. magnipapillata, N. vectensis, and A. digitifera, respectively. The mtDNA fraction covered by NUMTs was lower in N. vectensis (72.68%) and A. digitifera (0.47%) compared with H. magnipapillata (100%) (Table 1). NUMTs accounted for approximately 0.0470% (529,934 bp) of the H. magnipapillata genome (Table 1 and Figure 1C), which was much higher than the 0.0052% in N. vectensis (Table 1 and Figure 1B) and 0.00002% (86 bp) in A. digitifera (Table 1 and Figure 1A). The cumulative percentage was used as a measure of NUMT content in the genomes examined in this study, suggesting that the estimation of the NUMT content was not affected by differences in genome assembly fragmentation (Additional file 4: Table S5). Thus, although H. magnipapillata, N. vectensis, and A. digitifera belong to the same phylum, the NUMT compositions of the genomes of these three species are quite different. The number of NUMTs in the H. magnipapillata genome clearly exceeds those of the N. vectensis and A. digitifera genomes.


Exceptionally high cumulative percentage of NUMTs originating from linear mitochondrial DNA molecules in the Hydra magnipapillata genome.

Song S, Jiang F, Yuan J, Guo W, Miao Y - BMC Genomics (2013)

NUMT lengths distribution.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3716686&req=5

Figure 2: NUMT lengths distribution.
Mentions: We determined the homology relationships between the three cnidarian nuclear genomes and their corresponding mitochondrial genomes using BLASTN searches. A total of 704, 24 and 1 NUMTs were inferred in Hydra magnipapillata, Nematostella vectensis, and Acropora digitifera, respectively (Figure 1, Additional file 1: Table S1, Table S2, Additional file 2: Table S3, and Additional file 3: Table S4). The length distribution of the BLASTN hits was 51 to 7,684 bp (mean: 753 bp) for H. magnipapillata, 76 to 1,836 bp (mean: 768 bp) for N. vectensis, and 86 bp for A. digitifera (Figure 2). No obvious differences were observed in the length of NUMTs between H. magnipapillata and N. vectensis (mean lengths: 753 bp and 768 bp, respectively; Student’s t test: P = 0.8536), while their mean lengths were much longer than those observed in many other metazoans (e.g., Amphimedon queenslandica: 222 bp; Drosophila sechellia: 240 bp; Homo sapiens: 309 bp; Nasonia vitripenni: 565 bp) [5,35]. The largest proportion of NUMTs was between 100 and 200 bp in H. magnipapillata and between 800 and 900 bp in N. vectensis (Figure 2). The sequence similarity detected using BLASTN between NUMTs and homologous mtDNA sequences was 79.34 to 100%, 92.11 to 100%, and 95.35% in H. magnipapillata, N. vectensis, and A. digitifera, respectively. The mtDNA fraction covered by NUMTs was lower in N. vectensis (72.68%) and A. digitifera (0.47%) compared with H. magnipapillata (100%) (Table 1). NUMTs accounted for approximately 0.0470% (529,934 bp) of the H. magnipapillata genome (Table 1 and Figure 1C), which was much higher than the 0.0052% in N. vectensis (Table 1 and Figure 1B) and 0.00002% (86 bp) in A. digitifera (Table 1 and Figure 1A). The cumulative percentage was used as a measure of NUMT content in the genomes examined in this study, suggesting that the estimation of the NUMT content was not affected by differences in genome assembly fragmentation (Additional file 4: Table S5). Thus, although H. magnipapillata, N. vectensis, and A. digitifera belong to the same phylum, the NUMT compositions of the genomes of these three species are quite different. The number of NUMTs in the H. magnipapillata genome clearly exceeds those of the N. vectensis and A. digitifera genomes.

Bottom Line: We found that H. magnipapillata is an exceptional ancestral metazoan with a high NUMT cumulative percentage but a large genome, and its mitochondrial genome linearisation might be responsible for the NUMT enrichment.In addition, NUMT expression analyses showed that NUMTs are co-expressed with adjacent protein-coding genes, suggesting the relevance of their biological function.Taken together, our results provide valuable information for understanding the impact of mitochondrial genome structure on the interaction of mitochondrial molecules and nuclear genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming, Yunnan 650201, China.

ABSTRACT

Background: In contrast to most animal genomes, mitochondrial genomes in species belonging to the phylum Cnidaria show distinct variations in genome structure, including the mtDNA structure (linear or circular) and the presence or absence of introns in protein-coding genes. Therefore, the analysis of nuclear insertions of mitochondrial sequences (NUMTs) in cnidarians allows us to compare the NUMT content in animals with different mitochondrial genome structures.

Results: NUMT identification in the Hydra magnipapillata, Nematostella vectensis and Acropora digitifera genomes showed that the NUMT density in the H. magnipapillata genome clearly exceeds that in other two cnidarians with circular mitochondrial genomes. We found that H. magnipapillata is an exceptional ancestral metazoan with a high NUMT cumulative percentage but a large genome, and its mitochondrial genome linearisation might be responsible for the NUMT enrichment. We also detected the co-transposition of exonic and intronic fragments within NUMTs in N. vectensis and provided direct evidence that mitochondrial sequences can be transposed into the nuclear genome through DNA-mediated fragment transfer. In addition, NUMT expression analyses showed that NUMTs are co-expressed with adjacent protein-coding genes, suggesting the relevance of their biological function.

Conclusions: Taken together, our results provide valuable information for understanding the impact of mitochondrial genome structure on the interaction of mitochondrial molecules and nuclear genomes.

Show MeSH
Related in: MedlinePlus