Proper chloroplast biogenesis and function are essential for agriculture and life on earth because photosynthesis drives plant growth, development, and reproduction. Photosynthesis-related gene expression was previously reported to be induced by light signaling and repressed by plastid signaling. Although light signaling and plastid signaling were previously thought to independently regulate the expression of these genes, data indicating that the regulation of photosynthesis-related gene expression by light and plastid signals depends on common promoter elements led me to hypothesize that light signaling and plastid signaling might be interactive processes and that these interactions might be significant. I first tested this hypothesis by screening a group of Arabidopsis mutants with defects in plastid signaling for light signaling phenotypes. Based on results from these experiments, I conclude that the blue light receptor cryptochrome1 (cry1) contributes to both the light and the plastid signaling that regulates the expression of genes encoding the light-harvesting chlorophyll a/b-binding protein (Lhcb) of photosystem II. I provide evidence that plastid signaling broadly "rewires" light signaling and that in the case of the cry1 signaling that regulates Lhcb expression, this "rewiring" is largely caused by the conversion of long hypocotyl 5 (HY5) from a positive regulator to a negative regulator of Lhcb expression. HY5 is a bZIP-type transcription factor that acts downstream of cry1 and other photoreceptors. I found that cry1-dependent plastid signals are genetically distinct from GENOMES UNCOUPLED 1 (GUN1)-dependent plastid signals and that the interactions between light and plastid signals appear critical for proper chloroplast biogenesis. Addtionally, I found that plastid signals can broadly affect light-regulated development of Arabidopsis seedlings. Results from these developmental assays are consistent with cry1 and GUN1 helping integrate chloroplast function with light regulated development. Based on these findings, I hypothesized that the interactions between light and plastid signaling promote chloroplast biogenesis by optimizing the expression of chloroplast-related genes for particular light environments and that plastid signaling broadly regulates light signaling by affecting possibly numerous signaling factors that act downstream of photoreceptors. We tested these ideas with time-resolved- expression profiling. Results from the expression profiling are consistent with interactions between light and plastid signaling optimizing not only chloroplast biogenesis but also coordinating plant growth and development with chloroplast function. Results from the reverse genetic analyses of Arabidopsis mutants yielded mutant alleles that cause abnormal chloroplast biogenesis. These alleles have defects in eighteen genes that encode transcription factors, signaling factors, and proteins of no known function. These findings provide evidence that light and plastid signaling are interactive processes that not only promote chloroplast biogenesis and function but also affect diverse processes related to plant growth and development.
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