Assembly-controlled regulation of chloroplast gene translation

Abstract

Studies of the biogenesis of the photosynthetic protein complexes in the unicellular green alga Chlamydomonas reinhardtii have pointed to the importance of the concerted expression of nuclear and chloroplast genomes. The accumulation of chloroplast- and nuclear-encoded subunits is concerted, most often as a result of the rapid proteolytic disposal of unassembled subunits, but the rate of synthesis of some chloroplast-encoded subunits from photosynthetic protein complexes, designed as CES proteins (Controlled by Epistasy of Synthesis), is regulated by the availability of their assembly partners from the same complex. Cytochrome f, a major subunit of the cytochrome b(6)f complex is a model protein for the study of the CES process. In the absence of subunit IV, another subunit of the cytochrome b(6)f complex, its synthesis is decreased by 90%. This results from a negative autoregulation of cytochrome f translation initiation, mediated by a regulatory motif carried by the C-terminal domain of the unassembled protein [Choquet, Stern, Wostrikoff, Kuras, Girard-Bascou and Wollman (1998) Proc. Natl. Acad. Sci. U.S.A. 95, 4380-4385]. Using site-directed mutagenesis, we have characterized this regulatory motif. We discuss the possible implications regarding the mechanism of the CES process for cytochrome f expression. We have studied the possible generalization of this mechanism to other CES proteins.

Accumulation of the D2 Protein Is a Key Regulatory Step for Assembly of the Photosystem II Reaction Center Complex in Synechocystis PCC 6803

“…Regulation of D2 synthesis by the presence of cytochrome b 559 may correspond to a type of regulation previously described for cytochrome b 6 ⅐f assembly in the green alga Chlamydomonas. The absence of subunit IV of the cytochrome b 6 ⅐f complex was shown to down-regulate the synthesis of the cytochrome f protein (51). This concept of epistatic synthesis may prevent wasting energy for the synthesis of proteins that cannot be assembled.…”

A Conserved Mechanism Controls Translation of Rubisco Large Subunit in Different Photosynthetic Organisms

“…In higher plants and in green algae, expression of subunits that are part of large protein complexes is highly coordinated by CES (Choquet et al, 1998(Choquet et al, , 2001. The basis for this control system is that elimination of one subunit reduces the expression of other subunits in the complex by their translational arrest, or by degradation of unassembled subunits.…”

Chloroplast Biogenesis of Photosystem II Cores Involves a Series of Assembly-Controlled Steps That Regulate Translation

“…The molecular mechanism responsible for CES has been best characterized for cytochrome f from the cytochrome b 6 f complex. In the absence of its assembly partners, subunit IV or cytochrome b 6 , the synthesis of cytochrome f decreases 10-fold (Kuras and Wollman, 1994) as a result of an autoregulation of translation initiation (Choquet et al, 1998) mediated by the C-terminal domain of unassembled cytochrome f (Choquet et al, 2003). A similar mechanism controls the synthesis of PsaA and PsaC, two CES subunits from the photosystem I (PSI) complex (Wostrikoff et al, 2004).…”

“…However, its RNA binding property was not sequence specific (Yosef et al, 2004), a requirement for its contribution to the CES process. Therefore, as discussed for the biogenesis of other photosynthetic proteins (Choquet et al, 2003;Wostrikoff et al, 2004), this sequence specificity would rather be born by a ternary translational activator capable of competitive binding to both the unassembled CES subunit and the 59UTR of its target mRNA. This model sets translational efficiency to the rate of assembly of a CES subunit within a (sub)complex along the biogenesis pathway of a particular photosynthetic protein.…”

“…Most likely, assembly of the CES subunits in their target complex induces a proteasesensitive conformation that allows their proteolysis if PSII assembly cannot proceed further. Similarly, cytochrome f, a stable protein when unassembled (Kuras and Wollman, 1994;Choquet et al, 2003), becomes susceptible to proteolytic degradation upon nitrogen starvation once assembled within cytochrome b 6 f complexes (Bulte and Wollman, 1992).…”