Abstract
Plastids utilize a complex gene expression machinery, which has coevolved with the underlying genome sequence. Relatively, little is known about the genome-wide evolution of transcript processing in algal plastids that have undergone complex endosymbiotic events. We present the first genome-wide study of transcript processing in a plastid acquired through serial endosymbiosis, in the fucoxanthin-containing dinoflagellate Karlodinium veneficum. The fucoxanthin dinoflagellate plastid has an extremely divergent genome and utilizes two unusual transcript processing pathways, 3′-poly(U) tail addition and sequence editing, which were acquired following the serial endosymbiosis event. We demonstrate that poly(U) addition and sequence editing are widespread features across the Karl. veneficum plastid transcriptome, whereas other dinoflagellate plastid lineages that have arisen through independent serial endosymbiosis events do not utilize either RNA processing pathway. These pathways constrain the effects of divergent sequence evolution in fucoxanthin plastids, for example by correcting mutations in the genomic sequence that would otherwise be deleterious, and are specifically associated with transcripts that encode functional plastid proteins over transcripts of recently generated pseudogenes. These pathways may have additionally facilitated divergent evolution within the Karl. veneficum plastid. Transcript editing, for example, has contributed to the evolution of a novel C-terminal sequence extension on the Karl. veneficum AtpA protein. We furthermore provide the first complete sequence of an episomal minicircle in a fucoxanthin dinoflagellate plastid, which contains the dnaK gene, and gives rise to polyuridylylated and edited transcripts. Our results indicate that RNA processing in fucoxanthin dinoflagellate plastids is evolutionarily dynamic, coevolving with the underlying genome sequence.
Highlights
Plastid gene expression involves a complex set of transcriptional and post-transcriptional events
We present the first genome-wide study of transcript processing in a plastid acquired through serial endosymbiosis, in the fucoxanthin-containing dinoflagellate Karlodinium veneficum
We demonstrate that poly(U) addition and sequence editing are widespread features across the K. veneficum plastid transcriptome, whereas other dinoflagellate plastid lineages that have arisen through independent serial endosymbiosis events do not utilise either RNA processing pathway
Summary
Plastid gene expression involves a complex set of transcriptional and post-transcriptional events. Some of the features of plastid gene expression, such as the use of a bacterial RNA polymerase, and transcript cleavage, are likely to occur universally across the photosynthetic eukaryotes (Green 2011) Others, such as transcript splicing, sequence editing, and 3’ tail addition, appear to have evolved independently within individual plastid lineages (Asakura et al 2008; Lange et al 2009; Fujii and Small 2011), and this may be related to the evolution of the underlying genome sequence. The fucoxanthin-containing dinoflagellates possess serially acquired plastids derived from haptophyte algae (Takishita et al 1999; Gabrielsen et al 2011; Dorrell and Howe 2012). Plastid genome sequences have been assembled for the dinotom species Kryptoperidinium foliaceum and Durinskia baltica, and these retain far more genes, and are less divergent in content than the Karlodinium veneficum plastid genome (Imanian et al 2010; Gabrielsen et al 2011)
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