Establishment of photosynthesis through chloroplast development is controlled by two distinct regulatory phases

Abstract

Chloroplasts develop from undifferentiated proplastids present in meristematic tissue. Chloroplast biogenesis is thus closely connected to leaf development, which restricts our ability to study the process of chloroplast biogenesis per se. As a consequence we know relatively little about the regulatory mechanisms behind the establishment of the photosynthetic reactions and how the activities of the two genomes involved are coordinated during chloroplast development. We developed a single-cell-based experimental system from Arabidopsis with high temporal resolution allowing for investigations of the transition from proplastids to functional chloroplasts. Using this unique cell line we could show that establishment of photosynthesis is dependent on a regulatory mechanism involving two distinct phases. The first phase is triggered by rapid light-induced changes in gene expression and the metabolome. The second phase is dependent on the activation of the chloroplast and generates massive changes in nuclear gene expression required for the transition to photosynthetically functional chloroplasts.. The second phase is also associated with a spatial transition of the chloroplasts from clusters around the nucleus to the final position at the cell cortex. Thus, establishment of photosynthesis is a two-phase process with a clear checkpoint associated with the second regulatory phase allowing coordination of the activities of the nuclear and plastid genomes.