Permuted tRNA Genes in the Nuclear and Nucleomorph Genomes of Photosynthetic Eukaryotes

Permuted tRNA Genes in the Nuclear and Nucleomorph Genomes of Photosynthetic Eukaryotes
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DOI:
10.1093/molbev/msp313
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发表时间:
2010-05-01
影响因子:
10.7
通讯作者:
Nozaki, Hisayoshi
Nozaki, Hisayoshi
中科院分区:
生物学1区
文献类型:
--
作者:
Maruyama, Shinichiro;Sugahara, Junichi;Nozaki, Hisayoshi

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转移RNA(TRNA)是破译地球上所有生命形式基因组信息的核心遗传元件。然而,有大量缺失的tRNAs没有经过检查,特别是在微生物基因组中。已经报道了两个在结构和表达机制上有显著差异的tRNA基因家族:分裂tRNA和排列tRNAs。古生菌中分裂的tRNA在基因组上编码为两个或三个片段基因,然后加工成单个tRNA分子。排列的tRNA是由基因的5‘和3’半反向定位在基因组上的,到目前为止只在一个微小的红藻中发现。在这里,我们揭示了光合作用真核生物基因组中排列的tRNA基因的广泛分布。这包括迄今已知的最小的真核基因组--绿藻Bigelowiella Natans的核形态基因组。比较两个核形态编码的tRNA(Ser)基因的cDNA和基因组DNA序列,证实前体在体内被循环并加工成成熟的tRNA分子。在tRNA(Ser)(AGA)中,密码子摆动位置的腺嘌呤可能被修饰为肌苷,以扩大密码子的识别能力。我们还发现在超小型自由生活绿藻Ostreoins和Micromonas中存在排列的tRNAs,这两种藻类与B.Natans的核形态密切相关。含有内含子和排列的tRNA中保守的内含子/前导序列结构表明,真核生物和古生物的共同祖先中的剪接机制起源于古代。与此同时,光合作用真核生物中排列的tRNA基因的广泛但斑驳的分布表明,现存的排列的tRNA可能已经多次出现。综上所述,我们的数据表明,置换的tRNA是一个进化上保守的微小真核基因组中的基本元件。
Transfer RNA (tRNA) is a central genetic element in the decoding of genome information for all of Earth's life forms. Nevertheless, there are a great number of missing tRNAs that have been left without examination, especially in microbial genomes. Two tRNA gene families remarkable in their structure and expression mechanism have been reported: split and permuted tRNAs. Split tRNAs in archaea are encoded on the genome as two or three fragmented genes and then processed into single tRNA molecules. Permuted tRNAs are organized with the 5' and 3' halves of the gene positioned in reverse on the genome and hitherto have been found only in one tiny red alga. Here we reveal a wide-ranging distribution of permuted tRNA genes in the genomes of photosynthetic eukaryotes. This includes in the smallest eukaryotic genome known to date, the nucleomorph genome of the chlorarachniophyte alga Bigelowiella natans. Comparison between cDNA and genomic DNA sequences of two nucleomorph-encoded tRNA(Ser) genes confirms that precursors are circularized and processed into mature tRNA molecules in vivo. In the tRNA(Ser)(AGA), adenine at the wobble position of the codon is likely modified to inosine to expand capacity of the codon recognition. We also show the presence of permuted tRNAs in the ultrasmall free-living green algae Ostreococcus and Micromonas, which are closely related to the B. natans nucleomorph. Conserved intron/leader sequence structures in the intron-containing and permuted tRNAs suggest the ancient origin of the splicing machinery in the common ancestor of eukaryotes and archaea. Meanwhile, a wide but patchy distribution of permuted tRNA genes in the photosynthetic eukaryotes implies that extant permuted tRNAs might have emerged multiple times. Taken together, our data demonstrate that permuted tRNA is an evolutionarily conserved and fundamental element in tiny eukaryotic genomes.