Regulation of protochlorophyllide synthesis genes in darkness by class I TCP transcription factors TCP14 and TCP15 prevents photodamage after illumination in Arabidopsis.

De-etiolation, which takes place when seedlings germinated in the dark are first exposed to light, involves profound morphological and physiological changes, among them the synthesis of chlorophylls from the highly reactive precursor protochlorophyllide (Pchlide). As excess Pchlide accumulation can cause cellular damage upon illumination, the entire chlorophyll synthesis pathway is subjected to tight transcriptional control. Here, we report that the activity of the class I TCP transcription factors (TCPs) TCP14 and TCP15 is required to repress genes involved in Pchlide synthesis in the dark, thus contributing to successful de-etiolation. The TCPs improve the binding of PHYTOCHROME INTERACTING FACTOR 4 (PIF4), a repressor of Pchlide synthesis genes in darkness, to its target genes, possibly by affecting DELLA protein levels through changes in the expression of gibberellin synthesis genes. Moreover, protein-protein interaction studies in tobacco suggest that TCP15 may affect the formation of DELLA-PIF4 complexes, providing an additional possible mechanism for improving PIF4 action. Notably, the repressive effect of the TCPs is lost during de-etiolation and the TCPs behave as activators of Pchlide synthesis genes under illumination. This activation depends on the function of GOLDEN2-LIKE transcription factors, positive regulators of chloroplast biogenesis. In this way, the TCPs limit the synthesis of chlorophyll precursors in darkness, preventing photodamage during de-etiolation, but not under illumination conditions, when active chlorophyll synthesis is required.