SummaryDespite a strong interest in microalgal oil production, our understanding of the biosynthetic pathways that produce algal lipids and the genes involved in the biosynthetic processes remains incomplete. Here, we report that Chlamydomonas reinhardtii Cre09.g398289 encodes a plastid‐targeted 2‐lysophosphatidic acid acyltransferase (CrLPAAT1) that acylates the sn‐2 position of a 2‐lysophosphatidic acid to form phosphatidic acid, the first common precursor of membrane and storage lipids. In vitro enzyme assays showed that CrLPAAT1 prefers 16:0‐CoA to 18:1‐CoA as an acyl donor. Fluorescent protein‐tagged CrLPAAT1 was localized to the plastid membrane in C. reinhardtii cells. Furthermore, expression of CrLPAAT1 in plastids led to a > 20% increase in oil content under nitrogen‐deficient conditions. Taken together, these results demonstrate that CrLPAAT1 is an authentic plastid‐targeted LPAAT in C. reinhardtii, and that it may be used as a molecular tool to genetically increase oil content in microalgae.

Communication between organelles and the nucleus is referred to as anterograde (nucleus to organelle) and retrograde (organelle to nucleus) signalling. In plants, the pentatricopeptide repeat (PPR) proteins represent a large family of nuclear-encoded proteins that are required for post-transcriptional control of chloroplast and mitochondria gene expression, and hence play a central role in the nuclear anterograde control of organelle genome expression. How PPR gene expression is controlled and regulated by retrograde signals is, however, still unknown. Here, we report a significant role for the general transcription factor TFIIF α-subunit (TFIIFα) in controlling PPR gene expression in Arabidopsis. First, we found that TFIIFα interacts with the BIN4 subunit of the Topoisomerase VI (Topo VI). Transcriptome analysis of TFIIF and Topo VI mutant lines then revealed that many PLS-type PPR genes involved in RNA editing are reciprocally controlled by TFIIF and Topo VI. The misexpression of CLB19 and DYW1 genes in two allelic tfIIfα mutants was associated with editing impairments in their plastid target RNAs rpoA and ndhD, respectively. Interestingly, we also detected a change in NDH activity in tfIIfα plants. We also show that TFIIFα and Topo VI coordinate the expression of NDH subunits encoded by the nuclear and plastid genomes. These results reveal the crucial role of the nuclear TFIIFα and Topo VI complexes in controlling plastid genome expression at multiple levels of regulation, including the particular regulation of PPR gene expression.