Abstract

Plastid biogenesis and maintenance depend on the coordinated assembly of proteins imported from the cytosol with proteins translated within plastids. Chloroplasts in leaf cells have a greater need for protein import and protein synthesis than plastids in other organs due to the large amount of proteins required for photosynthesis. We previously reported that the Arabidopsis (Arabidopsis thaliana) transcription factor CIA2 specifically up-regulates leaf expression of genes encoding protein translocons Toc33 and Toc75, which are essential for protein import into chloroplasts. Protein import efficiency was therefore reduced in cia2 mutant chloroplasts. To further understand the function of CIA2, gene expression profiles of the wild type and a cia2 mutant were compared by microarray analysis. Interestingly, in addition to genes encoding protein translocon components, other genes down-regulated in cia2 almost exclusively encode chloroplast ribosomal proteins. Isolated cia2 mutant chloroplasts showed reduced translation efficiency and steady-state accumulation of plastid-encoded proteins. When CIA2 was ectopically expressed in roots, expression of both the protein translocon and ribosomal protein genes increased. Further analyses in vivo revealed that CIA2 up-regulated these genes by binding directly to their promoter regions. We propose that CIA2 is an important factor responsible for fulfilling the higher protein demands of leaf chloroplasts by coordinately increasing both protein import and protein translation efficiencies.

Highlights

  • Plastid biogenesis and maintenance depend on the coordinated assembly of proteins imported from the cytosol with proteins translated within plastids

  • In agreement with our previous data, TOC33 and TOC75 (AT3G46740, referred to as TOC75-III hereafter) were among the 38 genes down-regulated in cia2 (Table I)

  • Due to the demands of photosynthesis, leaf chloroplasts need to import more proteins than root plastids do. These photosynthesis-associated proteins are subsequently assembled with partner proteins produced within chloroplasts

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Summary

Introduction

Plastid biogenesis and maintenance depend on the coordinated assembly of proteins imported from the cytosol with proteins translated within plastids. We previously reported that the Arabidopsis (Arabidopsis thaliana) transcription factor CIA2 up-regulates leaf expression of genes encoding protein translocons Toc and Toc, which are essential for protein import into chloroplasts. Since leaf chloroplasts have a higher protein demand than plastids in other organs, both protein import and protein synthesis capacity should be upregulated in leaf chloroplasts How this coordinated up-regulation is achieved is not known. In addition to regulating the expression of translocon genes in leaves, CIA2 up-regulated expression of genes encoding chloroplast ribosomal proteins. This regulation appears to be direct because CIA2 was enriched in their promoter regions. We propose that CIA2 acts as a leaf-specific transcription factor to coordinately up-regulate protein import and protein. Ribosome biosynthesis AT1G32990 AT1G48350 AT2G33450 AT3G17170 AT3G25920 AT5G65220 AT2G38140 AT1G35680 AT1G74970 AT1G75350 AT2G43030 AT3G15190 AT3G44890 AT3G54210 AT4G01310 AT5G47190 AT5G51610

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