Feedback mechanisms are critical to the regulation of chloroplast development and signals from functional plastids are required to maintain nuclear gene expression of chloroplast proteins. To understand the role of these signals in de-etiolating Arabidopsis thaliana L. seedlings, we followed the expression of three nuclear genes, Lhcb, HEMA1 and GSA, under a variety of treatments (Norflurazon, lincomycin and a far-red light pre-treatment) leading to plastid damage in white light and in a range of genetic backgrounds known to modulate plastid signalling: the genomes uncoupled mutants, gun1, gun4, gun5 and the gun1,5 double mutant, and in a transgenic line over-expressing NADPH:protochlorophyllide oxidoreductase. The three nuclear genes were differentially sensitive to changes in plastid signalling, with Lhcb the most strongly repressed and GSA insensitive to all but the most severe treatments. Analysis of plastid morphology in seedlings grown under identical conditions demonstrated that these responses corresponded closely to the degree of plastid damage. Furthermore, although Lhcb and HEMA1 were responsive to both GUN1 and GUN5 signals, the relative inputs from these pathways differed for each transcript with GUN1 being dominant for HEMA1 regulation. Further analysis of HEMA1 expression in gun1 seedlings under non-photobleaching conditions indicates that GUN1 is an important suppressor of HEMA1 expression in the dark and under saturating white light. These results are consistent with plastid signals functioning in a feedback regulatory mechanism during chloroplast biogenesis, and suggest a key role for GUN1 during the early stages of chloroplast development.