Transcriptome analysis of respiration-responsive genes in Chlamydomonas reinhardtii: mitochondrial retrograde signaling coordinates the genes for cell proliferation with energy-producing metabolism.

Plant organelles are not only the recipients of signals from the nucleus, but also elicit signals to regulate nuclear genes; the latter process is called retrograde regulation. We previously reported a novel mitochondrial retrograde regulation in Chlamydomonas reinhardtii; nuclear photosynthesis genes are regulated in response to mitochondrial respiratory electron transport (RET). However, the physiological roles of this retrograde regulation are not yet fully understood. In this study, we performed a genome-wide transcriptome analysis of this alga to reveal what kinds of genes are responsive to this RET signal, using Chlamydomonas macroarrays containing 10,368 expressed sequence tag clones. From the analysis, we identified 147 inducible and 35 repressive genes based on a couple of criteria: induction/repression by activated respiration caused by exogenously added acetate, and the cancellations of these responses by treatment with antimycin A, an inhibitor of RET. Interestingly, genes for respiration, photosynthesis, glycolysis/gluconeogenesis, protein biosynthesis, cell wall biogenesis and flagella were significantly induced by RET-derived signals. From these findings, we discuss the physiological role of mitochondrial retrograde signaling in this unicellular alga, in terms of the coordination of cell proliferation with energy-producing metabolism.