A Bacterial-Type Sensor Kinase Couples Electron Transport to Gene Expression in Chloroplasts

Abstract

Two-component systems, comprising sensor histidine kinases and response regulators, are ubiquitous signal transducers in bacteria. Chloroplasts, despite having a cyanobacterial ancestry, do not appear to possess two-component systems as signal transducers. Apart from a few reported cases of two-component systems of the red algal chloroplasts, it is generally believed that the two-component systems of the ancestral symbiont were lost or recruited in various locations of the host cell other than chloroplasts. Here we report a typical bacterial-type sensor kinase in chloroplasts. The gene for this kinase is found in cyanobacteria, from which chloroplasts evolved, and has moved, in evolution, to the nuclear genomes of algae and green plants. The gene encoding this Chloroplast Sensor Kinase (CSK), when inactivated in Arabidopsis, results in plants that are disabled in photosynthetic control of chloroplast gene transcription. This CSK-dependent process requires a sensor of electron transport between chloroplast photosystems I and II. Thus CSK is involved in a redox regulatory mechanism that couples photosynthesis to chloroplast gene expression. Sequence similarity searches find homologues of CSK to be present in many different lineages of algae and plants and to be related phylogenetically to the known plastid two-component systems of red algae. The persistence of this ancient signalling system of cyanobacteria in chloroplasts and its function in coupling photosynthesis to chloroplast gene expression bears directly on the premise that chloroplasts retain genes whose expression must be regulated by photosynthetic electron transport and that the mechanism of regulation has been conserved from the prokaryotic, ancestral endosymbiont.