PHR1 mediates rapid high light responses and acclimation to high photosynthetic activity

Changing light intensity requires immediate metabolic adjustment which involves reprogramming of both plastidial and nuclear gene expression, but the signaling pathways behind such responses are not fully understood. Here we report that an increase in light intensity causes fluctuations of P_i levels in the chloroplasts of Arabidopsis thaliana and induces a transcriptional response mediated by the nuclear low-P_i signaling machinery involving the transcription factor PHOSPHATE STARVATION RESPONSE 1 (PHR1). Activation of PHR1 was linked to triose phosphate metabolism since the double mutant adg1 tpt-2, defective in both starch accumulation and triose phosphate export from the chloroplast, exhibited a constitutive transcriptional P_i starvation signature. Among the high light-induced target genes of PHR1, we further investigated SRG3/GDPD1, encoding an enzyme involved in phospholipid catabolism. Lipid profiling revealed pronounced changes in srg3 mutants compared with wild-type plants, including high light triggered accumulation of α-linolenic acid and reduced levels of the photoprotective carotenoid zeaxanthin. We propose that photosynthetic activity regulates the low-P_i response machinery in the nucleus in order to implement high light acclimation leading to the liberation of cellular P as well as the maintenance of membrane integrity.