Plastid RNA Polymerases in Higher Plants

Abstract

SummaryPlastids evolved from ancestral cyanobacteria through gradual conversion of an endosymbiont to a plant organelle. Plastids maintained a cyanobacterium-like (eubacterial) transcription machinery. The eubacterial core-enzyme consists of four plastid-encoded subunits (α2, β β′ and β″), and may associate with multiple, nuclear-encoded σ70-type specificity factors. This holo-enzyme is the plastid-encoded plastid RNA polymerase (PEP). The promoters recognized by the PEP are of σ70-type with conserved −10 (TATAAT) and −35 (TTGACA) elements. In addition, species-specific cis-elements and trans-factors regulate psbA, psbD and rrn16 promoter activity. The PEP in chloroplasts associates with up to eight auxiliary proteins. One of them is the plastid transcription kinase (PTK), an enzyme which regulates PEP transcription by σ factor phosphorylation. PTK activity itself is regulated by phosphorylation and the redox state of plastids.In addition to the eubacterial enzyme, plastids have acquired a second, phage-type RNA polymerase (NEP, nuclear-encoded plastid RNA polymerase). NEP probably evolved by duplication of the mitochondrial transcription machinery. A nuclear gene encodes the NEP catalytic core with a plastid targeting N-terminal sequence. The NEP subunit composition is likely to be similar to the mitochondrial enzyme, which associates with at least two specificity factors. NEP recognizes two distinct promoters. Type-I NEP promoters are ∼15 nt AT-rich region upstream (−14 to +1) of the transcription initiation site (+1) with a conserved YRTA core, a feature shared with plant mitochondrial promoters. Type-II NEP promoters are mainly downstream (−5 to +25) of the transcription initiation site.There is a division of labor between the two plastid RNA polymerases. Photosynthetic genes and operons have PEP promoters, whereas most non-photosynthetic genes involved in housekeeping functions, such as transcription and translation, have promoters for both RNA polymerases. The NEP promoter(s) of these genes are, with a few exceptions, silent in chloroplasts. Only a few genes are transcribed exclusively from a NEP promoter. One of these is the rpoB operon encoding three of the four PEP core subunits. Through transcription of the PEP genes by the NEP the nucleus indirectly controls transcription of plastid genes, there by integrating the endosymbiont-turned-organelle into the developmental network of multicellular plants.