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Chloroplast activities influence nuclear gene expression, a phenomenon referred to as retrograde signaling. Biogenic retrograde signals have been revealed by changes in nuclear gene expression when chloroplast development is disrupted. Research on biogenic signaling has focused on repression of Photosynthesis-Associated Nuclear Genes (PhANGs), but this is just one component of a syndrome involving altered expression of thousands of genes involved in diverse processes, many of which are upregulated. We discuss evidence for a framework that accounts for most of this syndrome. Disruption of chloroplast biogenesis prevents the production of signals required to progress through discrete steps in the program of photosynthetic differentiation, causing retention of juvenile states. As a result, expression of PhANGs and other genes that act late during photosynthetic differentiation is not initiated, while expression of genes that act early is retained. The extent of juvenility, and thus the transcriptome, reflects the disrupted process: lack of plastid translation blocks development very early, whereas disruption of photosynthesis without compromising plastid translation blocks development at a later stage. We discuss implications of these and other recent observations for the nature of the plastid-derived signals that regulate photosynthetic differentiation and the role of GUN1, an enigmatic protein involved in biogenic signaling., Competing Interests: Conflict of interest statement. None declared., (© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

Chloroplast biogenesis requires synthesis of proteins in the nucleocytoplasm and the chloroplast itself. Nucleus-encoded chloroplast proteins are imported via multiprotein translocons in the organelle's envelope membranes. Controversy exists around whether a 1-MDa complex comprising TIC20, TIC100, and other proteins constitutes the inner membrane TIC translocon. The Arabidopsis thaliana cue8 virescent mutant is broadly defective in plastid development. We identify CUE8 as TIC100. The tic100cue8 mutant accumulates reduced levels of 1-MDa complex components and exhibits reduced import of two nucleus-encoded chloroplast proteins of different import profiles. A search for suppressors of tic100cue8 identified a second mutation within the same gene, tic100soh1, which rescues the visible, 1 MDa complex-subunit abundance, and chloroplast protein import phenotypes. tic100soh1 retains but rapidly exits virescence and rescues the synthetic lethality of tic100cue8 when retrograde signaling is impaired by a mutation in the GENOMES UNCOUPLED 1 gene. Alongside the strong virescence, changes in RNA editing and the presence of unimported precursor proteins show that a strong signaling response is triggered when TIC100 function is altered. Our results are consistent with a role for TIC100, and by extension the 1-MDa complex, in the chloroplast import of photosynthetic and nonphotosynthetic proteins, a process which initiates retrograde signaling., (� The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

In darkness, shoot apex growth is repressed, but it becomes rapidly activated by light. We show that phytochromes and cryptochromes play largely redundant roles in this derepression in Arabidopsis thaliana. We examined the light activation of transcriptional changes in a finely resolved time course, comparing the shoot apex (meristem and leaf primordia) and the cotyledon and found >5700 differentially expressed genes. Early events specific to the shoot apices included the repression of genes for Really Interesting New Gene finger proteins and basic domain/leucine zipper and basic helix-loop-helix transcription factors. The downregulation of auxin and ethylene and the upregulation of cytokinin and gibberellin hormonal responses were also characteristic of shoot apices. In the apex, genes involved in ribosome biogenesis and protein translation were rapidly and synchronously induced, simultaneously with cell proliferation genes, preceding visible organ growth. Subsequently, the activation of signaling genes and transcriptional signatures of cell wall expansion, turgor generation, and plastid biogenesis were apparent. Furthermore, light regulates the forms and protein levels of two transcription factors with opposing functions in cell proliferation, E2FB and E2FC, through the Constitutively Photomorphogenic1 (COP1), COP9-Signalosome5, and Deetiolated1 light signaling molecules. These data provide the basis for reconstruction of the regulatory networks for light-regulated meristem, leaf, and cotyledon development.

Plastids are cellular organelles which originated when a photosynthetic prokaryote was engulfed by the eukaryotic ancestor of green and red algae and land plants. Plastids have diversified in plants from their original function as chloroplasts to fulfil a variety of other roles in metabolite biosynthesis and in storage, or purely to facilitate their own transmission, according to the cell type that harbours them. Therefore cellular development and plastid biogenesis pathways must be closely intertwined. Cell biological, biochemical, and genetic approaches have generated a large body of knowledge on a variety of plastid biogenesis processes. A brief overview of the components and functions of the plastid genetic machinery, the plastid division apparatus, and protein import to and targeting inside the organelle is presented here. However, key areas in which our knowledge is still surprisingly limited remain, and these are also discussed. Chloroplast-defective mutants suggest that a substantial number of important plastid biogenesis proteins are still unknown. Very little is known about how different plastid types differentiate, or about what mechanisms co-ordinate cell growth with plastid growth and division, in order to achieve what is, in photosynthetic cells, a largely constant cellular plastid complement. Further, it seems likely that major, separate plastid and chloroplast 'master switches' exist, as indicated by the co-ordinated gene expression of plastid or chloroplast-specific proteins. Recent insights into each of these developing areas are reviewed. Ultimately, this information should allow us to gain a systems-level understanding of the plastid-related elements of the networks of plant cellular development.