Abstract

BackgroundThe gene expression system of chloroplasts is far more complex than that of their cyanobacterial progenitor. This gain in complexity affects in particular RNA metabolism, specifically the transcription and maturation of RNA. Mature chloroplast RNA is generated by a plethora of nuclear-encoded proteins acquired or recruited during plant evolution, comprising additional RNA polymerases and sigma factors, and sequence-specific RNA maturation factors promoting RNA splicing, editing, end formation and translatability. Despite years of intensive research, we still lack a comprehensive explanation for this complexity.ResultsWe inspected the available literature and genome databases for information on components of RNA metabolism in land plant chloroplasts. In particular, new inventions of chloroplast-specific mechanisms and the expansion of some gene/protein families detected in land plants lead us to suggest that the primary function of the additional nuclear-encoded components found in chloroplasts is the transgenomic suppression of point mutations, fixation of which occurred due to an enhanced genetic drift exhibited by chloroplast genomes. We further speculate that a fast evolution of transgenomic suppressors occurred after the water-to-land transition of plants.ConclusionOur inspections indicate that several chloroplast-specific mechanisms evolved in land plants to remedy point mutations that occurred after the water-to-land transition. Thus, the complexity of chloroplast gene expression evolved to guarantee the functionality of chloroplast genetic information and may not, with some exceptions, be involved in regulatory functions.

Highlights

  • The gene expression system of chloroplasts is far more complex than that of their cyanobacterial progenitor

  • We propose that the evolution of RpoTs in plants, the expansion of the gene families coding for chloroplast sigma factors and pentatricopeptide repeat (PPR) proteins help to neutralize mutational lesions in the chloroplast genomes

  • We propose that PPR proteins are involved in neutralizing point mutations in coding regions, introns and UTRs, while different RNA polymerases and their co-factors help overcome problems caused by point mutations in promoter regions

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Summary

Introduction

The gene expression system of chloroplasts is far more complex than that of their cyanobacterial progenitor This gain in complexity affects in particular RNA metabolism, the transcription and maturation of RNA. Mature chloroplast RNA is generated by a plethora of nuclear-encoded proteins acquired or recruited during plant evolution, comprising additional RNA polymerases and sigma factors, and sequence-specific RNA maturation factors promoting RNA splicing, editing, end formation and translatability. BMC Biology 2008, 6:36 http://www.biomedcentral.com/1741-7007/6/36 genomes to date These sequences set to rest any remaining doubts that chloroplasts are ancient endosymbionts and are derived from cyanobacterial-like ancestors. The most puzzling of these was that the chloroplast gene expression system is far more complex than that of its cyanobacterial progenitors (Figure 1) This gain in complexity is due to changes in RNA metabolism, to novelties in the transcription and maturation of RNA. We propose a hypothesis on the origin of the complexity of chloroplast gene expression, encompassing recent data on factors involved in chloroplast transcription, RNA editing and RNA processing

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