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

doi:10.1016/j.cub.2018.06.006

Venkatasalam Shanmugabalaji, Hicham Chahtane + Show 5 more

Open Access

https://doi.org/10.1016/j.cub.2018.06.006

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Abstract

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 theimport 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.

Highlights

TOC159 and RGL2 Protein Levels Are Inversely Regulated during Seed Germination RGL2 plays a predominant role in repressing seedling establishment because RLG2 mRNA expression is positively regulated by abscisic acid (ABA), introducing a positive feedback loop sustaining high RGL2 accumulation [10,11,12]
The assembly of the photosynthetic apparatus during chloroplast biogenesis depends on the import of thousands of different preproteins by the chloroplast protein import machinery
Gibberellic acid (GA)-dependent downregulation of DELLA abundance is central in chlorophyll and carotenoid biosynthesis during the differentiation of functional chloroplasts and regulates chloroplast division and grana stacking in mesophyll cells [8, 9]

Summary

Introduction

TOC159 and RGL2 Protein Levels Are Inversely Regulated during Seed Germination RGL2 plays a predominant role in repressing seedling establishment because RLG2 mRNA expression is positively regulated by ABA, introducing a positive feedback loop sustaining high RGL2 accumulation [10,11,12]. Under unfavorable germination conditions, such as canopy light or high temperatures, GA synthesis is repressed, which promotes DELLA accumulation. To mimic those conditions, seeds were placed on MS medium containing paclobutrazol (PAC), an inhibitor of GA synthesis. We compared the effects of PAC on wild-type (WT) to those on the della single mutant rgl and the triple mutant rgl2/gai/rga, in which seedling germination and chloroplast biogenesis proceeds despite reduced concentrations of GA (Figure S1A). In PAC-treated WT seeds, TOC159 levels were strongly diminished when compared to untreated seeds, and in rgl and rgl2/gai/rga mutants, no PAC effects could be observed (Figures S1B and S1C).

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