Abstract

BackgroundReminiscent of their free-living cyanobacterial ancestor, chloroplasts proliferate by division coupled with the partition of nucleoids (DNA-protein complexes). Division of the chloroplast envelope membrane is performed by constriction of the ring structures at the division site. During division, nucleoids also change their shape and are distributed essentially equally to the daughter chloroplasts. Although several components of the envelope division machinery have been identified and characterized, little is known about the molecular components/mechanisms underlying the change of the nucleoid structure.ResultsIn order to identify new factors that are involved in the chloroplast division, we isolated Arabidopsis thaliana chloroplast division mutants from a pool of random cDNA-overexpressed lines. We found that the overexpression of a previously uncharacterized gene (AtYLMG1-1) of cyanobacterial origin results in the formation of an irregular network of chloroplast nucleoids, along with a defect in chloroplast division. In contrast, knockdown of AtYLMG1-1 resulted in a concentration of the nucleoids into a few large structures, but did not affect chloroplast division. Immunofluorescence microscopy showed that AtYLMG1-1 localizes in small puncta on thylakoid membranes, to which a subset of nucleoids colocalize. In addition, in the cyanobacterium Synechococcus elongates, overexpression and deletion of ylmG also displayed defects in nucleoid structure and cell division.ConclusionsThese results suggest that the proper distribution of nucleoids requires the YlmG protein, and the mechanism is conserved between cyanobacteria and chloroplasts. Given that ylmG exists in a cell division gene cluster downstream of ftsZ in gram-positive bacteria and that ylmG overexpression impaired the chloroplast division, the nucleoid partitioning by YlmG might be related to chloroplast and cyanobacterial division processes.

Highlights

  • Reminiscent of their free-living cyanobacterial ancestor, chloroplasts proliferate by division coupled with the partition of nucleoids (DNA-protein complexes)

  • Isolation of A. thaliana chloroplast division mutants from fulllength cDNA overexpresser (FOX) lines Several proteins required for chloroplast division have been identified and characterized by both forward and reverse genetics

  • Our results show that overexpression of AtYLMG1-1 protein causes formation of filamentous structure of chloroplast nucleoids, and that knockdown of AtYLMG1-1 causes the aggregation of nucleoids

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Summary

Introduction

Reminiscent of their free-living cyanobacterial ancestor, chloroplasts proliferate by division coupled with the partition of nucleoids (DNA-protein complexes). Division of the chloroplast envelope membrane is performed by constriction of the ring structures at the division site. Chloroplasts arose from a bacterial endosymbiont related to extant cyanobacteria. Chloroplasts are never synthesized de novo, but proliferate by division, reminiscent of their cyanobacterial ancestor. The chloroplast division process consists of a partitioning of nucleoids (DNA-protein complexes) and fission of the two envelope membranes. The envelope membrane fission event is performed by ring structures at the division site, encompassing both the inside and the outside of the two envelopes. Consistent with the endosymbiotic theory, the division ring contains nucleus-encoded homologs of cyanobacterial division proteins, such as FtsZ [2] and ARC6 [3].

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