Toward an Integrated Understanding of Retrograde Control of Photosynthesis

Significance: Photosynthesis takes place in the chloroplast of eukaryotes, which occupies a large portion of the photosynthetic cell. The chloroplast function and integrity depend on intensive material and signal exchange between all genetic compartments and conditionally secure efficient photosynthesis and high fitness. Recent Advances: During the last two decades, the concept of mutual control of plastid performance by extraplastidic anterograde signals acting on the chloroplast and the feedback from the chloroplast to the extraplastidic space by retrograde signals has been profoundly revised and expanded. It has become clear that a complex set of diverse signals is released from the chloroplast and exceeds the historically proposed small number of information signals. Thus, it is also recognized that redox compounds and reactive oxygen species play a decisive role in retrograde signaling. Critical Issues: The diversity of processes controlled or modulated by the retrograde network covers all molecular levels, including RNA fate and translation, and also includes subcellular heterogeneity, indirect gating of other organelles' metabolism, and specific signaling routes and pathways, previously not considered. All these processes must be integrated for optimal adjustment of the chloroplast processes. Thus, evidence is presented suggesting that retrograde signaling affects translation, stress granule, and processing body (P-body) dynamics. Future Directions: Redundancy of signal transduction elements, parallelisms of pathways, and conditionally alternative mechanisms generate a robust network and system that only tentatively can be assessed by use of single-site mutants.