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CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis.

ABSTRACT: We identified an Arabidopsis thaliana mutant, clumped chloroplasts 1 (clmp1), in which disruption of a gene of unknown function causes chloroplasts to cluster instead of being distributed throughout the cytoplasm. The phenotype affects chloroplasts and nongreen plastids in multiple organs and cell types, but is detectable only at certain developmental stages. In young leaf petioles of clmp1, where clustering is prevalent, cells lacking chloroplasts are detected, suggesting impaired chloroplast partitioning during mitosis. Although organelle distribution and partitioning are actin-dependent in plants, the actin cytoskeleton in clmp1 is indistinguishable from that in WT, and peroxisomes and mitochondria are distributed normally. A CLMP1-YFP fusion protein that complements clmp1 localizes to discrete foci in the cytoplasm, most of which colocalize with the cell periphery or with chloroplasts. Ultrastructural analysis revealed that chloroplasts within clmp1 clusters are held together by membranous connections, including thin isthmi characteristic of late-stage chloroplast division. This finding suggests that constriction of dividing chloroplasts proceeds normally in clmp1, but separation is impaired. Consistently, chloroplast size and number, as well as positioning of the plastid division proteins FtsZ and ARC5/DRP5B, are unaffected in clmp1, indicating that loss of CLMP1-mediated chloroplast separation does not prevent otherwise normal division. CLMP1-like sequences are unique to green algae and land plants, and the CLMP1 sequence suggests that it functions through protein-protein interactions. Our studies identify a unique class of proteins required for plastid separation after the constriction stage of plastid division and indicate that CLMP1 activity is also required for plastid distribution and partitioning during cell division.

SUBMITTER: Yang Y

PROVIDER: S-EPMC3215037 | biostudies-literature | 2011 Nov

REPOSITORIES: biostudies-literature

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CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis.

Yang Yue Y Sage Tammy L TL Liu Yi Y Ahmad Tiara R TR Marshall Wallace F WF Shiu Shin-Han SH Froehlich John E JE Imre Kathleen M KM Osteryoung Katherine W KW

Proceedings of the National Academy of Sciences of the United States of America 20111024 45

We identified an Arabidopsis thaliana mutant, clumped chloroplasts 1 (clmp1), in which disruption of a gene of unknown function causes chloroplasts to cluster instead of being distributed throughout the cytoplasm. The phenotype affects chloroplasts and nongreen plastids in multiple organs and cell types, but is detectable only at certain developmental stages. In young leaf petioles of clmp1, where clustering is prevalent, cells lacking chloroplasts are detected, suggesting impaired chloroplast p ...[more]

PMID: 22025705

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Project description:BACKGROUND: Plastids arose from a free-living cyanobacterial endosymbiont and multiply by binary division as do cyanobacteria. Plastid division involves nucleus-encoded homologs of cyanobacterial division proteins such as FtsZ, MinD, MinE, and ARC6. However, homologs of many other cyanobacterial division genes are missing in plant genomes and proteins of host eukaryotic origin, such as a dynamin-related protein, PDV1 and PDV2 are involved in the division process. Recent identification of plastid division proteins has started to elucidate the similarities and differences between plastid division and cyanobacterial cell division. To further identify new proteins that are required for plastid division, we characterized previously and newly isolated plastid division mutants of Arabidopsis thaliana. RESULTS: Leaf cells of two mutants, br04 and arc2, contain fewer, larger chloroplasts than those of wild type. We found that ARC2 and BR04 are identical to nuclear genes encoding the plastid chaperonin 60 alpha (ptCpn60alpha) and chaperonin 60 beta (ptCpn60beta) proteins, respectively. In both mutants, plastid division FtsZ ring formation was partially perturbed though the level of FtsZ2-1 protein in plastids of ptcpn60beta mutants was similar to that in wild type. Phylogenetic analyses showed that both ptCpn60 proteins are derived from ancestral cyanobacterial proteins. The A. thaliana genome encodes two members of ptCpn60alpha family and four members of ptCpn60beta family respectively. We found that a null mutation in ptCpn60alpha abolished greening of plastids and resulted in an albino phenotype while a weaker mutation impairs plastid division and reduced chlorophyll levels. The functions of at least two ptCpn60beta proteins are redundant and the appearance of chloroplast division defects is dependent on the number of mutant alleles. CONCLUSION: Our results suggest that both ptCpn60alpha and ptCpn60beta are required for the formation of a normal plastid division apparatus, as the prokaryotic counterparts are required for assembly of the cell division apparatus. Since moderate reduction of ptCpn60 levels impaired normal FtsZ ring formation but not import of FtsZ into plastids, it is suggested that the proper levels of ptCpn60 are required for folding of stromal plastid division proteins and/or regulation of FtsZ polymer dynamics.

Dataset Information

CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis.

Publications

CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis.

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