A chloroplast’s biography: how genetics uncovered a tale of light and a developmental checkpoint

Chloroplasts sustain life on Earth. They represent the photosynthetic and ancestral form of the family of plastids in all plant cells, which include proplastids in undifferentiated stem cells, and primed but photosynthetically-incompetent “etioplasts” in the dark. This substantially explains why light exposure of dark-grown seedlings triggers a vast reprogramming of the plant’s transcriptome. Monocot leaves display a developmental gradient revealing phases of plastid proliferation, assembly of the endogenous transcription and translation apparatus and pigment and membrane components, and eventually greening. Disruptions of these stages have uncovered developmental checkpoints, including one which arguably underlies the phenomenon long referred to as “plastid biogenic retrograde signalling”. We highlight plastid roles in distinct cell types, summarise the chloroplast developmental sequence, review the mutant screens for chloroplast-related light signalling and what they taught us, address the unexpected observations in chloroplast developmental mutants which could be explained by the checkpoint model, and propose that light control of chloroplast biogenesis evolved through co-option in angiosperms of a pre-existing, safeguarding developmental checkpoint mechanism during the proplastid-to-chloroplast sequence, which itself evolved as pluricellular plant meristems did. In tribute to Joanne Chory, we reflect on the value of carefully-designed and interpreted mutant screens to our understanding of chloroplast biology.