Two-component signalling systems of chloroplasts: function, distribution and evolution

Abstract

Two-component signal transduction, comprising sensor kinases and response regulators, is the predominant signalling mechanism in prokaryotes. This signalling system originated in bacteria, and has spread to the eukaryotic domain of life through symbiotic, lateral gene transfer from the bacterial ancestors of chloroplasts and mitochondria. During the course of their evolution, chloroplasts, with the exception of a few instances in non-green algae, appear to have relinquished all genes encoding two-component systems to their eukaryotic host cell nuclei. In green algae and plants, chloroplast genes for two-component systems were neither known nor were chloroplast two-component proteins shown to exist as products of nuclear genes prior to the work described here. This thesis describes the identification and characterisation of a novel two-component sensor kinase in chloroplasts. This Chloroplast Sensor Kinase (CSK) is the product of a nuclear gene in algae and plants. CSK is synthesised in the cytosol of Arabidopsis thaliana and imported into the chloroplast as a protein precursor. CSK is autophosphorylated and couples photosynthetic electron transport to gene transcription in chloroplasts. The identity of the response regulator partner of CSK reveals an unexpected phylogenetic and functional relatedness of CSK with chloroplast two-component systems of non-green algae. Chloroplast two-component systems are likely to be universal in photosynthetic eukaryotes and they persist in chloroplasts as products of nuclear genes even where chloroplast genomes no longer encode them. Chloroplast twocomponent systems have homologues in extant cyanobacterial lineages, indicating their ancient cyanobacterial origin. The persistence of cyanobacterial two-component systems in chloroplasts and their function in coupling photosynthesis with chloroplast gene expression are central to the premise that chloroplasts retain genes whose expression is regulated by the activity of the photosynthetic electron transport chain, using a mechanism conserved from their cyanobacterial ancestors.