Chloroplast Biogenesis Controlled by DELLA-TOC159 Interaction in Early Plant Development

Venkatasalam Shanmugabalaji, Hicham Chahtane, Sonia Accossato, Michèle Rahire, Guillaume Gouzerh, Luis Lopez-Molina, Felix Kessler

Chloroplast biogenesis, visible as greening, is the key to photoautotrophic growth in plants. At the organelle level, it requires the development of non-photosynthetic, color-less proplastids to photosynthetically active, green chloroplasts at early stages of plant development, i.e., in germinating seeds. This depends on the import of thousands of different preproteins into the developing organelle by the chloroplast protein import machinery [1]. The preprotein import receptor TOC159 is essential in the process, its mutation blocking chloroplast biogenesis and resulting in albino plants [2]. The molecular mechanisms controlling the onset of chloroplast biogenesis during germination are largely unknown. Germination depends on the plant hormone gibberellic acid (GA) and is repressed by DELLA when GA concentrations are low [3, 4]. Here, we show that DELLA negatively regulates TOC159 protein abundance under low GA. The direct DELLA-TOC159 interaction promotes TOC159 degradation by the ubiquitin/proteasome system (UPS). Moreover, the accumulation of photosynthesis-associated proteins destined for the chloroplast is downregulated posttranscriptionally. Analysis of a model import substrate indicates that it is targeted for removal by the UPS prior to import. Thus, under low GA, the UPS represses chloroplast biogenesis by a dual mechanism comprising the DELLA-dependent destruction of the import receptor TOC159, as well as that of its protein cargo. In conclusion, our data provide a molecular framework for the GA hormonal control of proplastid to chloroplast transition during early plant development.