However, as seeds most often germinate underneath soil, seedling development typically begins in darkness and follows a skotomorphogenic program called etiolation, characterized by rapid hypocotyl elongation and etioplast development. For seeds that germinate in the light, chloroplasts may differentiate directly from proplastids present in cotyledons. Light is a crucial factor for chloroplast differentiation. Seedling development relies on successful chloroplast biogenesis, ensuring the transition from heterotrophic to autotrophic growth. Altogether, we establish a roadmap for chloroplast differentiation, a critical process for plant photoautotrophic growth and survival. Moreover, these data detail thylakoid membrane expansion during de-etiolation at the seedling level and the relative contribution and differential regulation of proteins and lipids at each developmental stage. This showed two distinct phases of chloroplast biogenesis: an initial photosynthesis-enabling ‘Structure Establishment Phase’ followed by a ‘Chloroplast Proliferation Phase’ during cell expansion. Furthermore, we used quantitative lipid and whole proteome data to complement the (ultra)structural data, providing a time-resolved, multi-dimensional description of chloroplast differentiation. Using Serial Block Face Scanning Electron Microscopy (SBF-SEM), we generated a series of chloroplast 3D reconstructions during differentiation, revealing chloroplast number and volume and the extent of envelope and thylakoid membrane surfaces. However, the sequence of events during chloroplast differentiation remains poorly understood. Light triggers chloroplast differentiation whereby the etioplast transforms into a photosynthesizing chloroplast and the thylakoid rapidly emerges.
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