Abstract
Cytochrome oxidase subunit 3 (Cox3) is a mitochondrion-encoded core membrane protein of complex IV of the mitochondrial respiratory chain, and consists of seven trans-membrane helices. Here we show that in diverse later-branching dinoflagellates, cox3 is consistently split into two exons in the mitochondrial genome between helices six and seven. Gene exons are transcribed as two discrete oligoadenylated precursor RNAs, and these are subsequently trans-spliced to form a complete coding mRNA. This trans-splicing is highly unusual in that some of the oligoadenylated tail is incorporated at the splice site, such that a short string of adenosines links the two coding exons. This feature is consistently represented in diverse dinoflagellates, however the number of adenosines added varies according to the size of the coding gap between the two exons. Thus we observed between zero (Amphidinium carterae) and 10 (Symbiodinium sp.) adenosines added in different taxa, but the final coding sequence length is identical with the reading frame maintained. Northern analyses show that precursor cox3 transcripts are approximately equally abundant as mature cox3 mRNAs, suggesting a slow or regulated maturation process. These data indicate that the splicing mechanism in dinoflagellate mitochondria is tolerant of variations in the length of the precursor coding sequence, and implicates the use of a splicing template, or guide molecule, during splicing that controls mature mRNA length.
Highlights
The expression pathway from gene to protein is not always a simple one
The remainder of cox3 occurs as a separate gene fragment, and a transcript of this fragment was presumed to complete the mRNA [17,18]. Two features of this trans-splicing case are unusual: 1) no genomic sequence around the splice sites could be identified that could participate in a known splicing reaction such as group I/II intron fragments, or bulgehelix-bulge formation; and 2) five, non-encoded adenosine nucleotides bridge the gap in cox3 transcripts between the two gene exons, presumably donated from the oligoadenosine tail of the 731-nucleotide transcript [17]
The break in coding sequence in K. veneficum cox3 occurs between transmembrane helices six and seven, so we define the two gene exons as cox3H1-6, and cox3H7
Summary
The expression pathway from gene to protein is not always a simple one. One of the most common elaborations on the geneRtranscriptRprotein dogma is the presence of introns which break up otherwise contiguous coding sequences within a genome, and which must be removed by cis-splicing of the gene transcript [1]. Two features of this trans-splicing case are unusual: 1) no genomic sequence around the splice sites could be identified that could participate in a known splicing reaction such as group I/II intron fragments, or bulgehelix-bulge formation; and 2) five, non-encoded adenosine nucleotides bridge the gap in cox3 transcripts between the two gene exons (nts 1–731, 737–858), presumably donated from the oligoadenosine tail of the 731-nucleotide transcript [17].
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