The OPR Protein MTHI1 Controls the Expression of Two Different Subunits of ATP Synthase CFo in Chlamydomonas reinhardtii

In Chlamydomonas reinhardtii, chloroplast gene expression is tightly regulated post-transcriptionally by gene-specific trans-acting protein factors. Here we report the identification of an OctotricoPeptide Repeat (OPR) protein, MDH1, critical for the biogenesis of chloroplast ATP synthase CF0. At variance with most trans-acting factors characterised so far in C. reinhardtii that control the expression of a single gene, MDH1 targets two distinct transcripts: it is required for the accumulation and the translation of the atpH mRNA, encoding a subunit of the selective proton channel but it also enhances the translation of the atpI mRNA, which encodes the other subunit of the channel. MDH1 targets the 59UTR of both atpH and atpI genes. Co-immuno-precipitation and small RNA sequencing revealed that MDH1 binds specifically a sequence highly conserved among Chlorophyceae and the Ulvale clade of Ulvophyceae at the 59end of the tri-phosphorylated atpH mRNA. A very similar sequence, located about 60 nt upstream of the atpI initiation codon, was also conserved in some Chlorophyceae and Ulvale species and was found essential for atpI mRNA translation in C. reinhardtii. Such a dual targeted trans-acting factor, thus provides a mean to co-regulate the expression of the two proton hemi-channels.