PHR1 and PHL1 mediate rapid high-light responses and acclimation to triose phosphate oversupply

Abstract

Fluctuations in light intensity require immediate metabolic adjustment which includes reprogramming of both plastidial and nuclear gene expression, but the signaling pathways behind such responses are not fully understood. Here we report the identification of an early high-light responsive pathway in Arabidopsis thaliana that depends on PHOSPHATE STARVATION RESPONSE 1 (PHR1) and PHR1-LIKE 1 (PHL1) transcription factors involved in low phosphate (Pi) signaling. High-light treatment rapidly induced the accumulation of PHR1-responsive transcripts in wildtype plants grown under nutrient-sufficient conditions, but not in phr1 phl1 double knockout plants. Differences in starch accumulation and ATP levels were detected between wildtype and phr1 phl1 mutants subjected to high light, suggesting a link between Pi signaling, carbohydrate partitioning, and energy status during stress. In line with a function of PHR1/PHL1 upon triose phosphate accumulation, we observed that blocking starch biosynthesis in the phr1 phl1 double mutant, by introducing the agd1-1 allele, causes a severe growth defect. Phenotypes of the adg1 phr1 phl1 triple mutant such as high-light sensitivity and growth restriction in the absence of exogenously supplied sucrose resemble the previously described double mutant adg1 tpt-2, lacking a functional copy of the TRIOSE PHOSPHATE/PHOSPHATE TRANSLOCATOR (TPT), and we show that Pi responses are disturbed in adg1 tpt-2. We propose that Pi sequestration by photosynthesis and import of Pi into the chloroplast transiently depletes cytosolic Pi reserves upon sudden increases in light intensity. The low-Pi sensing machinery in the nucleus consequently implements early high-light transcriptional responses, qualifying Pi as a new operational retrograde signal.