TRANSLATION OF CYTOCHROME-F IS AUTOREGULATED THROUGH THE 5'-UNTRANSLATED REGION OF PETA MESSENGER-RNA IN CHLAMYDOMONAS CHLOROPLASTS

A process that we refer to as control by epistasy of synthesis (CES pr ocess) occurs during chloroplast protein biogenesis in Chlamydomonas r einhardtii: the synthesis of some chloroplast-encoded subunits, the CE S subunits, is strongly attenuated when some other subunits from the s ame complex, the dominant subunits, are missing. Herein we investigate the molecular basis of the CES process for the biogenesis of the cyto chrome b(6)f complex and show that negative autoregulation of cytochro me f translation occurs in the absence of other complex subunits. This autoregulation is mediated by an interaction, either direct or indire ct, between the 5' untranslated region of petA mRNA which encodes cyto chrome f, and the C-terminal domain of the unassembled protein. This m odel for the regulation of cytochrome f translation explains both the decreased rate of cytochrome f synthesis in vivo in the absence of its assembly partners and its increase in synthesis when significant accu mulation of the C-terminal domain of the protein is prevented. When ex pressed from a chimeric mRNA containing the atpA 5' untranslated regio n, cytochrome f no longer showed an assembly-dependent regulation of t ranslation. Conversely, the level of antibiotic resistance conferred b y a chimeric petA-aadA-rbcL gene was shown to depend on the state of a ssembly of cytochrome b(6)f complexes and on the accumulation of the C -terminal domain of cytochrome f. We discuss the possible ubiquity of the CES process in organellar protein biogenesis.