Mechanisms for maintenance, replication, and repair of the chloroplast genome in plants

Nielsen, Brent L.; Cupp, John D.; Brammer, Jeffrey M.

doi:10.1093/jxb/erq163

Cited by 23 publications

(16 citation statements)

References 17 publications

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“…Our understanding of plant organelle DNA replication is still very incomplete (Bendich, 2007;Nielsen et al, 2010). This is largely due to our ignorance concerning some of the most basic factors, such as DNA polymerases, that contribute to this fundamental process in plants.…”

Section: Discussion An Essential Role For the Poli Genes In Higher Plmentioning

confidence: 99%

Divergent Roles for the Two PolI-Like Organelle DNA Polymerases of Arabidopsis

2011

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DNA polymerases play a central role in the process of DNA replication. Yet, the proteins in charge of the replication of plant organelle DNA have not been unambiguously identified. There are however many indications that a family of proteins homologous to bacterial DNA polymerase I (PolI) is implicated in organelle DNA replication. Here, we have isolated mutant lines of the PolIA and PolIB genes of Arabidopsis (Arabidopsis thaliana) to test this hypothesis. We find that mutation of both genes is lethal, thus confirming an essential and redundant role for these two proteins. However, the mutation of a single gene is sufficient to cause a reduction in the levels of DNA in both mitochondria and plastids. We also demonstrate that polIb, but not polIa mutant lines, are hypersensitive to ciprofloxacin, a small molecule that specifically induces DNA double-strand breaks in plant organelles, suggesting a function for PolIB in DNA repair. In agreement with this result, a cross between polIb and a plastid Whirly mutant line yielded plants with high levels of DNA rearrangements and severe growth defects, indicating impairments in plastid DNA repair pathways. Taken together, this work provides further evidences for the involvement of the plant PolI-like genes in organelle DNA replication and suggests an additional role for PolIB in DNA repair.

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Section: Discussion An Essential Role For the Poli Genes In Higher Plmentioning

confidence: 99%

Divergent Roles for the Two PolI-Like Organelle DNA Polymerases of Arabidopsis

2011

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“…Each plastid contains multiple copies of the genome which are distributed among a variable number of nucleoids. Despite the growing number of proteins shown to play roles in DNA replication and maintenance (Maréchal and Brisson, 2010), the mechanism of ptDNA replication is yet not well understood and might depend on the developmental stage of plastids (Nielsen et al, 2010). In fact, several mechanisms of DNA replication were proposed and one involves a chloroplast-targeted RecA protein (Rowan et al, 2010).…”

Section: Dna Organization In Plastidsmentioning

confidence: 99%

Dynamic composition, shaping and organization of plastid nucleoids

et al. 2014

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In this article recent progress on the elucidation of the dynamic composition and structure of plastid nucleoids is reviewed from a structural perspective. Plastid nucleoids are compact structures of multiple copies of different forms of ptDNA, RNA, enzymes for replication and gene expression as well as DNA binding proteins. Although early electron microscopy suggested that plastid DNA is almost free of proteins, it is now well established that the DNA in nucleoids similarly as in the nuclear chromatin is associated with basic proteins playing key roles in organization of the DNA architecture and in regulation of DNA associated enzymatic activities involved in transcription, replication, and recombination. This group of DNA binding proteins has been named plastid nucleoid associated proteins (ptNAPs). Plastid nucleoids are unique with respect to their variable number, genome copy content and dynamic distribution within different types of plastids. The mechanisms underlying the shaping and reorganization of plastid nucleoids during chloroplast development and in response to environmental conditions involve posttranslational modifications of ptNAPs, similarly to those changes known for histones in the eukaryotic chromatin, as well as changes in the repertoire of ptNAPs, as known for nucleoids of bacteria. Attachment of plastid nucleoids to membranes is proposed to be important not only for regulation of DNA availability for replication and transcription, but also for the coordination of photosynthesis and plastid gene expression.

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“…Kolodner and Tewari (1975) also reported evidence for rolling circle replication upon completion of replication of a ctDNA molecule by the D-loop mechanism. This suggests that, similar to some phage systems, ctDNA may replicate by more than one mechanism (Nielsen et al 2010). This is supported by studies from the Koop laboratory that show that targeted inactivation of either or both of the D-loop replication origins was not lethal, although some of the mutants generated led to reduced plant growth rate and reduced ctDNA copy number per cell (Muhlbauer et al 2002;Scharff and Koop 2007).…”

mentioning

confidence: 95%

“…These reports suggest that D-loop replication may play a role in only certain stages of plant growth, such as maintenance of ctDNA in mature cells. The early rapid expansion of ctDNA may be facilitated by rolling circle or recombination-dependent DNA replication (Nielsen et al 2010;Scharff and Koop 2006;Bendich 2003, 2004). Rolling circle replication has also been observed in plant mitochondria (Backert et al 1996).…”

mentioning

confidence: 99%

Identification of a soybean chloroplast DNA replication origin-binding protein

2011

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Replication of chloroplast DNA (ctDNA) in several plants and in Chlamydomonas reinhardii has been shown to occur by a double displacement loop (D-loop) mechanism and potentially also by a rolling circle mechanism. D-loop replication origins have been mapped in several species. Minimal replication origin sequences used as probes identified two potential binding proteins by southwestern blot analysis. A 28 kDa (apparent molecular weight by SDS-PAGE analysis) soybean protein has been isolated by origin sequence-specific DNA affinity chromatography from total chloroplast proteins. Mass spectrometry analysis identified this protein as the product of the soybean C6SY33 gene (accession number ACU14156), which is annotated as encoding a putative uncharacterized protein with a molecular weight of 25,897 Da, very near the observed molecular weight of the purified protein based on gel electrophoresis. Western blot analysis using an antibody against a homologous Arabidopsis protein indicates that this soybean protein is localized specifically in chloroplasts. The soybean protein shares some homology within a single-stranded DNA binding (SSB) domain of E. coli SSB and an Arabidopsis thaliana mitochondrial-localized SSB of about 21 kDa (mtSSB). However, the soybean protein induces a specific electrophoretic mobility shift only when incubated with a double-stranded fragment containing the previously mapped ctDNA replication oriA region. This protein has no electrophoretic mobility shift activity when incubated with single-stranded DNA. In contrast, the Arabidopsis mtSSB causes a mobility shift only with single-stranded DNA but not with the oriA fragment or with control dsDNA of unrelated sequence. These results suggest that the 26 kDa soybean protein is a specific origin binding protein that may be involved in initiation of ctDNA replication.

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Mechanisms for maintenance, replication, and repair of the chloroplast genome in plants

Cited by 23 publications

References 17 publications

Divergent Roles for the Two PolI-Like Organelle DNA Polymerases of Arabidopsis

Divergent Roles for the Two PolI-Like Organelle DNA Polymerases of Arabidopsis

Dynamic composition, shaping and organization of plastid nucleoids

Identification of a soybean chloroplast DNA replication origin-binding protein

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