Elsevier

Journal of Plant Physiology

Volume 168, Issue 12, 15 August 2011, Pages 1345-1360
Journal of Plant Physiology

Review
The transcription machineries of plant mitochondria and chloroplasts: Composition, function, and regulation

https://doi.org/10.1016/j.jplph.2011.01.005Get rights and content

Summary

Although genomes of mitochondria and plastids are very small compared to those of their bacterial ancestors, the transcription machineries of these organelles are of surprising complexity. With respect to the number of different RNA polymerases per organelle, the extremes are represented on one hand by chloroplasts of eudicots which use one bacterial-type RNA polymerase and two phage-type RNA polymerases to transcribe their genes, and on the other hand by Physcomitrella possessing three mitochondrial RNA polymerases of the phage type. Transcription of genes/operons is often driven by multiple promoters in both organelles. This review describes the principle components of the transcription machineries (RNA polymerases, transcription factors, promoters) and the division of labor between the different RNA polymerases. While regulation of transcription in mitochondria seems to be only of limited importance, the plastid genes of higher plants respond to exogenous and endogenous cues rather individually by altering their transcriptional activities.

Introduction

Mitochondria and plastids possess their own genomes and transcription machineries. Although both organelles preserve features of eubacterial genomes, they have acquired, during their evolution, specialized components for gene expression, which are encoded in the nucleus. During the co-evolution of plastids (cyanobacterial endosymbiont) and the eukaryotic host cell massive losses of genes from the chondrome (mitochondrial genome) and plastome (plastid genome) have occurred (Martin et al., 2002, Dyall et al., 2004, Gray, 2004, Gray, 2010, Knoop, 2004, Richly and Leister, 2004, Brandvain and Wade, 2009). However, the cells did not lose all of those genes, since thousands of them have been transferred to the nucleus, still a relatively frequent and ongoing process (Brennicke et al., 1993, Martin and Herrmann, 1998, Palmer et al., 2000, Herrmann et al., 2003, Martin, 2003, Adams and Daley, 2004, Timmis et al., 2004, Leister, 2005, Stegemann and Bock, 2006). A considerable number of proteins encoded by those genes were rerouted back into the plastids/mitochondria by acquiring plastid and/or mitochondrial targeting sequences. In a similar way, many nuclear-encoded proteins of non-organellar origin also became part of the organellar proteome (eukaryotization; Sato, 2001, Hengeveld and Fedonkin, 2004). This eukaryotization is also reflected by the transcriptional machineries of mitochondria and plastids in higher plants. Considering the small sizes of the chondromes and plastomes of higher plants compared to the genomes of their bacterial ancestors, the transcriptional machineries of mitochondria and even more of plastids are surprisingly complex. Here we describe the different components of the transcriptional machinery in mitochondria and plastids and their roles in transcription and its regulation.

Section snippets

Mitochondrial RNA polymerases are phage-type enzymes

Mitochondrial transcription is performed by nuclear-encoded phage-type RNA polymerase(s) (RNAP(s); reviewed in Tracy and Stern, 1995, Hess and Börner, 1999, Weihe, 2004, Liere and Börner, 2011). The protist Reclinomonas americana is the only known organism which has retained the ancestral bacterial RNAP genes in its chondrome (Lang et al., 1997). While most eukaryotes including also algae and the lycophyte Selaginella moellendorffii (Yin et al., 2009) possess only one nuclear gene for a (in

PEP: the plastid-encoded plastid RNA polymerase

The plastomes of algae and higher plants possess rpoA, rpoB, rpoC1, and rpoC2 genes for core subunits of a cyanobacterial-type RNA polymerase, which is commonly abbreviated as PEP (plastid-encoded plastid RNA polymerase; Lysenko and Kuznetsov, 2005, Shiina et al., 2005, Liere and Börner, 2007a, Liere and Börner, 2007b). PEP ß- and ß′-subunits can functionally substitute homologous subunits of the E. coli RNA polymerase (Severinov et al., 1996). Furthermore, PEP exhibits sensitivity to

Acknowledgements

The work of the authors is supported by Deutsche Forschungsgemeinschaft (SFB 429). We thank Kristina Kühn for providing initial artwork.

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