To cope with environmental stresses, plants often adopt a memory response upon primary stress exposure to facilitate a quicker and stronger reaction to recurring stresses. However, it remains unknown whether light is involved in the manifestation of stress memory. Proline accumulation is a striking metabolic adaptation of higher plants during various environmental stresses. Here we show that salinity-induced proline accumulation is memorable and HY5-dependent light signaling is required for such a memory response. Primary salt stress induced the expression of Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1), encoding a proline biosynthetic enzyme and proline accumulation, which were reduced to basal level during the recovery stage. Reoccurring salt stress-induced stronger P5CS1 expression and proline accumulation were dependent upon light exposure during the recovery stage. Further studies demonstrated that salt-induced transcriptional memory of P5CS1 is associated with the retention of increased H3K4me3 level at P5CS1 during the recovery stage. HY5 binds directly to light-responsive element, C/A-box, in the P5CS1 promoter. Deletion of the C/A-box or hy5 hyh mutations caused rapid reduction of H3K4me3 level at P5CS1 during the recovery stage, resulting in impairment of the stress memory response. These results unveil a previously unrecognized mechanism whereby light regulates salt-induced transcriptional memory via the function of HY5 in maintaining H3K4me3 level at the memory gene.
Keywords: H3K4me3; HY5/HYH; P5CS1; light; transcriptional memory.