Abstract
Organelle genes are often interrupted by group I and or group II introns. Splicing of these mobile genetic occurs at the RNA level via serial transesterification steps catalyzed by the introns'own tertiary structures and, sometimes, with the help of external factors. These catalytic ribozymes can be found in cis or trans configuration, and although trans-arrayed group II introns have been known for decades, trans-spliced group I introns have been reported only recently. In the course of sequencing the complete mitochondrial genome of the prasinophyte picoplanktonic green alga Prasinoderma coloniale CCMP 1220 (Prasinococcales, clade VI), we uncovered two additional cases of trans-spliced group I introns. Here, we describe these introns and compare the 54,546 bp-long mitochondrial genome of Prasinoderma with those of four other prasinophytes (clades II, III and V). This comparison underscores the highly variable mitochondrial genome architecture in these ancient chlorophyte lineages. Both Prasinoderma trans-spliced introns reside within the large subunit rRNA gene (rnl) at positions where cis-spliced relatives, often containing homing endonuclease genes, have been found in other organelles. In contrast, all previously reported trans-spliced group I introns occur in different mitochondrial genes (rns or coxI). Each Prasinoderma intron is fragmented into two pieces, forming at the RNA level a secondary structure that resembles those of its cis-spliced counterparts. As observed for other trans-spliced group I introns, the breakpoint of the first intron maps to the variable loop L8, whereas that of the second is uniquely located downstream of P9.1. The breakpoint In each Prasinoderma intron corresponds to the same region where the open reading frame (ORF) occurs when present in cis-spliced orthologs. This correlation between the intron breakpoint and the ORF location in cis-spliced orthologs also holds for other trans-spliced introns; we discuss the possible implications of this interesting observation for trans-splicing of group I introns.
Highlights
Group I and group II introns are mobile genetic elements frequently encountered in mitochondrial and plastid genomes [1]
Group I and group II introns are generally capable of self-splicing through a series of transesterification reactions, which can be further facilitated in vivo by a maturase encoded within an open reading frame (ORF) present in the intron or by a splicing factor encoded elsewhere in the organelle genome or the nuclear genome [2,3]
While trans-spliced group II introns have been known for decades [7,8], the first trans-spliced group I introns were reported in 2009 [9,10], with only a few additional cases documented since their discoveries [11,12,13,14]
Summary
Group I and group II introns are mobile genetic elements frequently encountered in mitochondrial and plastid genomes [1]. They propagate to cognate and ectopic sites via homing and transposition processes. The intron is split into non-adjacent pieces that are often far apart in the genome and located on different strands. These intron pieces flanked by exon sequences must interact at the RNA level to produce a functional intron structure that allows splicing to take place; the separate primary transcripts derived from the individual exon sequences are joined and ligated after assembly and splicing of the flanking intron sequences. In the trans-spliced introns whose secondary structures have been predicted, the junction between the 59 and 39 fragments, i.e. the breakpoint, is usually located in the loop subtending the base-paired region P8 (L8) [9,13,14]; the orthologous cox introns found in the lycophytes Isoetes engelmannii/
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