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Published on: July 29, 2019
Alterations in rRNA-mRNA interaction during plastid evolution
Kyungtaek Lim1, Ichizo Kobayashi1, Kenta Nakai2
1Department of Medical Genome Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Minato-ku, Tokyo, JapanThe Institute of Medical Science, The University of Tokyo, Minato-ku, Tokyo, Japan.
Abstract:
Translation initiation depends on the recognition of mRNA by a ribosome. For this to occur, prokaryotes primarily use the Shine-Dalgarno (SD) interaction, where the 3'-tail of small subunit rRNA (core motif: 3'CCUCC) forms base pairs with a complementary signal sequence in the 5'-untranslated region of mRNA. Here, we examined what happened to SD interactions during the evolution of a cyanobacterial endosymbiont into modern plastids (including chloroplasts). Our analysis of available complete plastid genome sequences revealed that the majority of plastids retained SD interactions but with varying levels of usage. Parallel losses of SD interactions took place in plastids of Chlorophyta, Euglenophyta, and Chromerida/Apicomplexa lineages, presumably related to their extensive reductive evolution. Interestingly, we discovered that the classical SD interaction (3'CCUCC/5'GGAGG [rRNA/mRNA]) was replaced by an altered SD interaction (3'CCCU/5'GGGA or 3'CUUCC/5'GAAGG) through coordinated changes in the sequences of the core rRNA motif and its paired mRNA signal. These changes in plastids of Chlorophyta and Euglenophyta proceeded through intermediate stages that allowed both the classical and altered SD interactions. This coevolution between the rRNA motif and the mRNA signal demonstrates unexpected plasticity in the translation initiation machinery.
Insights
Plastids retain Shine-Dalgarno interactions for translation initiation, with some lineages evolving altered interactions. This demonstrates the adaptability of the translation machinery during organelle evolution.
Area of Science:
- Molecular Biology
- Evolutionary Biology
- Genomics
Background:
- Translation initiation in prokaryotes relies on Shine-Dalgarno (SD) interactions between ribosomal RNA and mRNA.
- This interaction involves base pairing between the 3'-tail of small subunit rRNA (core motif: 3'CCUCC) and a complementary sequence in the mRNA's 5'-untranslated region.
Purpose of the Study:
- To investigate the evolutionary fate of Shine-Dalgarno interactions during the transition of cyanobacterial endosymbionts to modern plastids.
- To analyze the conservation and variation of SD interactions across diverse plastid lineages.
Main Methods:
- Analysis of complete plastid genome sequences from various lineages.
- Comparative genomics to identify conserved and divergent sequences in rRNA and mRNA involved in translation initiation.
Main Results:
- Most plastids maintain SD interactions, though usage varies significantly.
- SD interactions were lost in plastids of Chlorophyta, Euglenophyta, and Chromerida/Apicomplexa, correlating with reductive evolution.
- An altered SD interaction (3'CCCU/5'GGGA or 3'CUUCC/5'GAAGG) replaced the classical one (3'CCUCC/5'GGAGG) in some lineages, involving coordinated sequence changes in rRNA and mRNA.
Conclusions:
- Plastid evolution exhibits plasticity in translation initiation, with evidence of both retention and modification of SD interactions.
- Coevolution between the rRNA motif and mRNA signal highlights the dynamic nature of the translational machinery.
- Intermediate stages suggest a gradual evolutionary process for the altered SD interactions in Chlorophyta and Euglenophyta.
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