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A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.).

Tanaka Y, Tsuda M, Yasumoto K, Yamagishi H, Terachi T - BMC Genomics (2012)

Bottom Line: Ogura-type mitochondrial genome has four unique regions (2,803 bp, 1,601 bp, 451 bp and 15,255 bp in size) that are non-syntenic to normal-type genome, and the gene orf138 was found to be located at the edge of the largest unique region.Blast analysis performed to assign the unique regions showed that about 80% of the region was covered by short homologous sequences to the mitochondrial sequences of normal-type radish or other reported Brassicaceae species, although no homology was found for the remaining 20% of sequences.Ogura-type mitochondrial genome was highly rearranged compared with the normal-type genome by recombination through one large repeat and multiple short repeats.

View Article: PubMed Central - HTML - PubMed

Affiliation: 31 Laboratory, Kyoto Sangyo University, Motoyama, Kamigamo, Kita-ku, Kyoto 603-8555, Japan. terachi@cc.kyoto-su.ac.jp

ABSTRACT

Background: Plant mitochondrial genome has unique features such as large size, frequent recombination and incorporation of foreign DNA. Cytoplasmic male sterility (CMS) is caused by rearrangement of the mitochondrial genome, and a novel chimeric open reading frame (ORF) created by shuffling of endogenous sequences is often responsible for CMS. The Ogura-type male-sterile cytoplasm is one of the most extensively studied cytoplasms in Brassicaceae. Although the gene orf138 has been isolated as a determinant of Ogura-type CMS, no homologous sequence to orf138 has been found in public databases. Therefore, how orf138 sequence was created is a mystery. In this study, we determined the complete nucleotide sequence of two radish mitochondrial genomes, namely, Ogura- and normal-type genomes, and analyzed them to reveal the origin of the gene orf138.

Results: Ogura- and normal-type mitochondrial genomes were assembled to 258,426-bp and 244,036-bp circular sequences, respectively. Normal-type mitochondrial genome contained 33 protein-coding and three rRNA genes, which are well conserved with the reported mitochondrial genome of rapeseed. Ogura-type genomes contained same genes and additional atp9. As for tRNA, normal-type contained 17 tRNAs, while Ogura-type contained 17 tRNAs and one additional trnfM. The gene orf138 was specific to Ogura-type mitochondrial genome, and no sequence homologous to it was found in normal-type genome. Comparative analysis of the two genomes revealed that radish mitochondrial genome consists of 11 syntenic regions (length >3 kb, similarity >99.9%). It was shown that short repeats and overlapped repeats present in the edge of syntenic regions were involved in recombination events during evolution to interconvert two types of mitochondrial genome. Ogura-type mitochondrial genome has four unique regions (2,803 bp, 1,601 bp, 451 bp and 15,255 bp in size) that are non-syntenic to normal-type genome, and the gene orf138 was found to be located at the edge of the largest unique region. Blast analysis performed to assign the unique regions showed that about 80% of the region was covered by short homologous sequences to the mitochondrial sequences of normal-type radish or other reported Brassicaceae species, although no homology was found for the remaining 20% of sequences.

Conclusions: Ogura-type mitochondrial genome was highly rearranged compared with the normal-type genome by recombination through one large repeat and multiple short repeats. The rearrangement has produced four unique regions in Ogura-type mitochondrial genome, and most of the unique regions are composed of known Brassicaceae mitochondrial sequences. This suggests that the regions unique to the Ogura-type genome were generated by integration and shuffling of pre-existing mitochondrial sequences during the evolution of Brassicaceae, and novel genes such as orf138 could have been created by the shuffling process of mitochondrial genome.

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A possible model for integration of the sequence (unique region IV) in Ogura-type mitochondrial genome. Yellow small arrows indicate identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp inverted repeats is present (purple small arrows). Unique region IV had been integrated into radish mitochondria genome via these repeats when recombination between syntenic regions 7 and 11 occurred.
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Figure 5: A possible model for integration of the sequence (unique region IV) in Ogura-type mitochondrial genome. Yellow small arrows indicate identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp inverted repeats is present (purple small arrows). Unique region IV had been integrated into radish mitochondria genome via these repeats when recombination between syntenic regions 7 and 11 occurred.

Mentions: The sequence of Ogura-type unique region IV can be derived from a mixture of sequences in the reported Brassicaceae mitochondrial genome. The next question relates to how this unique region IV was generated or integrated into the radish mitochondrial genome. We searched for repeated sequences around this region. Ogura-type unique region IV was shown to be sandwiched between syntenic regions 7 and 11 (Figure 5). There were identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp repeated sequences was found in inverted orientation. These 28-bp sequences are specific to the Ogura-type mitochondrial genome, and not found in normal-type genome. This characteristic arrangement of repeats indicates that unique region IV was integrated into the radish mitochondrial genome when recombination between syntenic regions 7 and 11 occurred.


A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.).

Tanaka Y, Tsuda M, Yasumoto K, Yamagishi H, Terachi T - BMC Genomics (2012)

A possible model for integration of the sequence (unique region IV) in Ogura-type mitochondrial genome. Yellow small arrows indicate identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp inverted repeats is present (purple small arrows). Unique region IV had been integrated into radish mitochondria genome via these repeats when recombination between syntenic regions 7 and 11 occurred.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3473294&req=5

Figure 5: A possible model for integration of the sequence (unique region IV) in Ogura-type mitochondrial genome. Yellow small arrows indicate identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp inverted repeats is present (purple small arrows). Unique region IV had been integrated into radish mitochondria genome via these repeats when recombination between syntenic regions 7 and 11 occurred.
Mentions: The sequence of Ogura-type unique region IV can be derived from a mixture of sequences in the reported Brassicaceae mitochondrial genome. The next question relates to how this unique region IV was generated or integrated into the radish mitochondrial genome. We searched for repeated sequences around this region. Ogura-type unique region IV was shown to be sandwiched between syntenic regions 7 and 11 (Figure 5). There were identical 176-bp inverted repeats at the edges of regions 7 and 11. On the insides of these repeated sequences, another pair of 28-bp repeated sequences was found in inverted orientation. These 28-bp sequences are specific to the Ogura-type mitochondrial genome, and not found in normal-type genome. This characteristic arrangement of repeats indicates that unique region IV was integrated into the radish mitochondrial genome when recombination between syntenic regions 7 and 11 occurred.

Bottom Line: Ogura-type mitochondrial genome has four unique regions (2,803 bp, 1,601 bp, 451 bp and 15,255 bp in size) that are non-syntenic to normal-type genome, and the gene orf138 was found to be located at the edge of the largest unique region.Blast analysis performed to assign the unique regions showed that about 80% of the region was covered by short homologous sequences to the mitochondrial sequences of normal-type radish or other reported Brassicaceae species, although no homology was found for the remaining 20% of sequences.Ogura-type mitochondrial genome was highly rearranged compared with the normal-type genome by recombination through one large repeat and multiple short repeats.

View Article: PubMed Central - HTML - PubMed

Affiliation: 31 Laboratory, Kyoto Sangyo University, Motoyama, Kamigamo, Kita-ku, Kyoto 603-8555, Japan. terachi@cc.kyoto-su.ac.jp

ABSTRACT

Background: Plant mitochondrial genome has unique features such as large size, frequent recombination and incorporation of foreign DNA. Cytoplasmic male sterility (CMS) is caused by rearrangement of the mitochondrial genome, and a novel chimeric open reading frame (ORF) created by shuffling of endogenous sequences is often responsible for CMS. The Ogura-type male-sterile cytoplasm is one of the most extensively studied cytoplasms in Brassicaceae. Although the gene orf138 has been isolated as a determinant of Ogura-type CMS, no homologous sequence to orf138 has been found in public databases. Therefore, how orf138 sequence was created is a mystery. In this study, we determined the complete nucleotide sequence of two radish mitochondrial genomes, namely, Ogura- and normal-type genomes, and analyzed them to reveal the origin of the gene orf138.

Results: Ogura- and normal-type mitochondrial genomes were assembled to 258,426-bp and 244,036-bp circular sequences, respectively. Normal-type mitochondrial genome contained 33 protein-coding and three rRNA genes, which are well conserved with the reported mitochondrial genome of rapeseed. Ogura-type genomes contained same genes and additional atp9. As for tRNA, normal-type contained 17 tRNAs, while Ogura-type contained 17 tRNAs and one additional trnfM. The gene orf138 was specific to Ogura-type mitochondrial genome, and no sequence homologous to it was found in normal-type genome. Comparative analysis of the two genomes revealed that radish mitochondrial genome consists of 11 syntenic regions (length >3 kb, similarity >99.9%). It was shown that short repeats and overlapped repeats present in the edge of syntenic regions were involved in recombination events during evolution to interconvert two types of mitochondrial genome. Ogura-type mitochondrial genome has four unique regions (2,803 bp, 1,601 bp, 451 bp and 15,255 bp in size) that are non-syntenic to normal-type genome, and the gene orf138 was found to be located at the edge of the largest unique region. Blast analysis performed to assign the unique regions showed that about 80% of the region was covered by short homologous sequences to the mitochondrial sequences of normal-type radish or other reported Brassicaceae species, although no homology was found for the remaining 20% of sequences.

Conclusions: Ogura-type mitochondrial genome was highly rearranged compared with the normal-type genome by recombination through one large repeat and multiple short repeats. The rearrangement has produced four unique regions in Ogura-type mitochondrial genome, and most of the unique regions are composed of known Brassicaceae mitochondrial sequences. This suggests that the regions unique to the Ogura-type genome were generated by integration and shuffling of pre-existing mitochondrial sequences during the evolution of Brassicaceae, and novel genes such as orf138 could have been created by the shuffling process of mitochondrial genome.

Show MeSH
Related in: MedlinePlus