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Light triggers chloroplast differentiation in dark grown (etiolated) seedlings. A precursor organelle, the etioplast, transforms into a photosynthesizing chloroplast. Over the course of just a few hours, an extensive photosynthetic membrane system, the thylakoid, emerges. This requires synthesis of highly abundant membrane lipids as well as specific photosynthesis-associated proteins. But the sequence of events during chloroplast differentiation is still unclear. Using Serial Block Face Scanning Microscopy (SBF-SEM) we generated a time course of 3D reconstructions of entire cells and chloroplasts during differentiation, revealing number, volume as well as envelope and thylakoid membrane surface. The (ultra)structural data are completed with quantitative lipid and whole proteome data that together provide a time-resolved, multi-dimensional analysis of chloroplast biogenesis. Our data reveal the differential regulation of galactolipid synthesis pathways and sequential activation of photosystems. The superimposition of the structural and biochemical data reveals two distinct phases; an initial “Structure Establishment Phase” enabling onset of photosynthesis, followed by a “Chloroplast Proliferation Phase” coinciding with cell expansion. Thereby we establish a roadmap to chloroplast biogenesis, a critical process towards photoautotrophic growth and survival of young plants.

Authors of the study:

Rosa Pipitone¹, Simona Eicke², Barbara Pfister², Gaetan Glauser³, Denis Falconet⁴, Thibaut Pralon¹, Sam Zeeman², Felix Kessler¹, Emilie Demarsy^1,5

¹ Plant physiology laboratory, University of Neuchâtel, Neuchâtel, Switzerland
² Institute of Agricultural Sciences, Department of Biology ETH Zurich, Zurich, Switzerland
³ Neuchâtel Platform of Analytical Chemistry, University of Neuchâtel, Neuchâtel, Switzerland
⁴ Laboratoire de Physiologie Cellulaire et Végétale, Institut National de Recherche Agronomique, Commissariat à l'Energie Atomique et aux Energies Alternatives, Grenoble, France
⁵ Department of Botany and Plant Biology, University of Geneva, CH-1211 Geneva 4, Switzerland