The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts

Abstract

We describe a novel, typically prokaryotic, sensor kinase in chloroplasts of green plants. The gene for this chloroplast sensor kinase (CSK) is found in cyanobacteria, prokaryotes from which chloroplasts evolved. The CSK gene has moved, during evolution, from the ancestral chloroplast to the nuclear genomes of eukaryotic algae and green plants. The CSK protein is now synthesised in the cytosol of photosynthetic eukaryotes and imported into their chloroplasts as a protein precursor. In the model higher plant Arabidopsis thaliana, CSK is autophosphorylated and required for control of transcription of chloroplast genes by the redox state of an electron carrier connecting photosystems I and II. CSK therefore provides a redox regulatory mechanism that couples photosynthesis to gene expression. This mechanism is inherited directly from the cyanobacterial ancestor of chloroplasts, is intrinsic to chloroplasts, and is targeted to chloroplast genes. cell evolution ͉ chloroplast genome ͉ redox ͉ transcription ͉ two-component system

The Phosphorylation Status of the Chloroplast Protein Kinase STN7 of Arabidopsis Affects Its Turnover

“…The fact that the decline of STN7 under state 1 conditions occurred as in the wild type in the stn8 mutant suggests that the STN8 kinase is probably not involved in STN7 phosphorylation. Similar conclusion can be reached for the CSK kinase (Puthiyaveetil et al, 2008) from the observation that in its absence the decrease of STN7 still Figure 5. The decrease of STN7 under state 1 conditions is blocked in the STN7-4D lines.…”

Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment

“…Other chloroplast protein kinases have been identified and characterized, including the casein kinase CKII (involved in the control of chloroplast gene expression [56]), the CSK kinase (which has also been proposed to control gene expression through redox control [57] although the evidence is still sparse) and the TAK1 kinase [58,59] (which has been proposed to phosphorylate LHCII). Unfortunately, no further studies have been performed with this kinase.…”

“…The PPH1 and the PBCP phosphatases act as the counterparts of the Stt7/STN7 and Stl1/STN8 kinases, respectively [53][54][55]. The kinases CK2a and CSK act on the chloroplast gene expression system and may be redox-controlled [56,57]. TAK1 has been proposed to be involved in LHCII phosphorylation but its precise role remains to be determined [58,59].…”

ArabidopsisSTN7 Kinase Provides a Link between Short- and Long-Term Photosynthetic Acclimation

“…One branch concerns chloroplast gene expression (chloroplast branch) and is responsible for the transcriptional regulation of PSI-related genes, such as the psaAB operon. The chloroplast sensor kinase (CSK) (Puthiyaveetil et al, 2008), reported to regulate the transcription of psaAB operon, might be a component of the chloroplast branch. A second branch might be responsible for the regulation of the accumulation of products of nuclear photosynthesis-related genes (nucleus-cytosol branch).…”

“…Our analyses allowed to exclude the TSP9 protein as a possible component of the LTR signaling pathway. A possible candidate might be the chloroplast sensor kinase, shown to couple the redox state of the PQ pool with the expression of chloroplast photosynthesisrelated genes (Puthiyaveetil et al, 2008;Figure 12). In the future, phosphoproteomic studies of chloroplast proteins, comparing wild-type and stn7-1 mutant plants, exposed to light conditions favoring PSI or PSII complexes, appears to be the strategy of choice to identify as yet unknown proteins that, upon phosphorylation, might relay the signal to other regions of the chloroplast and to the nucleus.…”