Chloroplast DNA Replication Is Regulated by the Redox State Independently of Chloroplast Division in <i>Chlamydomonas reinhardtii</i>

Kabeya, Yukihiro; Miyagishima, Shin-ya

doi:10.1104/pp.113.216291

Cited by 30 publications

(26 citation statements)

References 53 publications

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“…It has been reported that the activity of plastid POP is regulated by the redox state in the green alga Chlamydomonas reinhardtii . In vivo and in vitro experiments have indicated that plastid DNA replication was activated and inactivated by artificially changing the cellular redox state, though the POP protein level was constant [43]. In some primary plastid-bearing algae, it is therefore possible that dual-localized POPs are independently activated by the redox state in each organelle, causing kinetic differences in organellar DNA replication.…”

Section: Discussionmentioning

confidence: 99%

Organellar DNA Polymerases in Complex Plastid-Bearing Algae

Hirakawa

Watanabe

2019

Biomolecules

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DNA replication in plastids and mitochondria is generally regulated by nucleus-encoded proteins. In plants and red algae, a nucleus-encoded enzyme called POP (plant and protist organellar DNA polymerase) is involved in DNA replication in both organelles by virtue of its dual localization. POPs are family A DNA polymerases, which include bacterial DNA polymerase I (PolI). POP homologs have been found in a wide range of eukaryotes, including plants, algae, and non-photosynthetic protists. However, the phylogeny and subcellular localizations of POPs remain unclear in many algae, especially in secondary and tertiary plastid-bearing groups. In this study, we report that chlorarachniophytes possess two evolutionarily distinct POPs, and fluorescent protein-tagging experiments demonstrate that they are targeted to the secondary plastids and mitochondria, respectively. The timing of DNA replication is different between the two organelles in the chlorarachniophyte Bigelowiella natans, and this seems to be correlated to the transcription of respective POP genes. Dinoflagellates also carry two distinct POP genes, possibly for their plastids and mitochondria, whereas haptophytes and ochrophytes have only one. Therefore, unlike plants, some algal groups are likely to have evolved multiple DNA polymerases for various organelles. This study provides a new insight into the evolution of organellar DNA replication in complex plastid-bearing organisms.

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Section: Discussionmentioning

confidence: 99%

Organellar DNA Polymerases in Complex Plastid-Bearing Algae

Hirakawa

Watanabe

2019

Biomolecules

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“…In green plants, such as wheat, barley and pea, the plastid DNA number varies during the developmental stages [ 39 – 44 ], suggesting that the frequency of DNA replication and plastid division changes at each stage. Additionally, in the unicellular algae Chlamydomonas reinhardtii , which contain one plastid per cell, the plastid DNA replicates multiples times before plastid division [ 45 ]. In addition, phosphate limitation strongly affects the copy number of plastid DNA in Chlamydomonas [ 46 ].…”

Section: Discussionmentioning

confidence: 99%

Intensive DNA Replication and Metabolism during the Lag Phase in Cyanobacteria

et al. 2015

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Unlike bacteria such as Escherichia coli and Bacillus subtilis, several species of freshwater cyanobacteria are known to contain multiple chromosomal copies per cell, at all stages of their cell cycle. We have characterized the replication of multi-copy chromosomes in the cyanobacterium Synechococcus elongatus PCC 7942 (hereafter Synechococcus 7942). In Synechococcus 7942, the replication of multi-copy chromosome is asynchronous, not only among cells but also among multi-copy chromosomes. This suggests that DNA replication is not tightly coupled to cell division in Synechococcus 7942. To address this hypothesis, we analysed the relationship between DNA replication and cell doubling at various growth phases of Synechococcus 7942 cell culture. Three distinct growth phases were characterised in Synechococcus 7942 batch culture: lag phase, exponential phase, and arithmetic (linear) phase. The chromosomal copy number was significantly higher during the lag phase than during the exponential and linear phases. Likewise, DNA replication activity was higher in the lag phase cells than in the exponential and linear phase cells, and the lag phase cells were more sensitive to nalidixic acid, a DNA gyrase inhibitor, than cells in other growth phases. To elucidate physiological differences in Synechococcus 7942 during the lag phase, we analysed the metabolome at each growth phase. In addition, we assessed the accumulation of central carbon metabolites, amino acids, and DNA precursors at each phase. The results of these analyses suggest that Synechococcus 7942 cells prepare for cell division during the lag phase by initiating intensive chromosomal DNA replication and accumulating metabolites necessary for the subsequent cell division and elongation steps that occur during the exponential growth and linear phases.

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“…Light has been shown to affect the amount of chloroplast DNA (ctDNA) during plant development (Shaver et al, 2008 ). Evidence for regulation of chloroplast DNA (ctDNA) by the redox state of cells has been reported in Chlamydomonas reinhardtii (Kabeya and Miyagishima, 2013 ), and similarly for yeast mitochondrial DNA (mtDNA; Hori et al, 2009 ).…”

Section: Introductionmentioning

confidence: 94%

Chloroplast DNA Copy Number Changes during Plant Development in Organelle DNA Polymerase Mutants

Morley

Nielsen

2016

Front. Plant Sci.

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Chloroplast genome copy number is very high in leaf tissue, with upwards of 10,000 or more copies of the chloroplast DNA (ctDNA) per leaf cell. This is often promoted as a major advantage for engineering the plastid genome, as it provides high gene copy number and thus is expected to result in high expression of foreign proteins from integrated genes. However, it is also known that ctDNA copy number and ctDNA integrity decrease as cells age. Quantitative PCR (qPCR) allows measurement of organelle DNA levels relative to a nuclear gene target. We have used this approach to determine changes in copy number of ctDNA relative to the nuclear genome at different ages of Arabidopsis plant growth and in organellar DNA polymerase mutants. The mutant plant lines have T-DNA insertions in genes encoding the two organelle localized DNA polymerases (PolIA and PolIB). Each of these mutant lines exhibits some delay in plant growth and development as compared to wild-type plants, with the PolIB plants having a more pronounced delay. Both mutant lines develop to maturity and produce viable seeds. Mutants for both proteins were observed to have a reduction in ctDNA and mtDNA copy number relative to wild type plants at all time points as measured by qPCR. Both DNA polymerase mutants had a fairly similar decrease in ctDNA copy number, while the PolIB mutant had a greater effect of reduction in mtDNA levels. However, despite similar decreases in genome copy number, RT-PCR analysis of PolIA mutants show that PolIB expression remains unchanged, suggesting that PolIA may not be essential to plant survival. Furthermore, genotypic analysis of plants from heterozygous parents display a strong pressure to maintain two functioning copies of PolIB. These results indicate that the two DNA polymerases are both important in ctDNA replication, and they are not fully redundant to each other, suggesting each has a specific function in plant organelles.

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Chloroplast DNA Replication Is Regulated by the Redox State Independently of Chloroplast Division in Chlamydomonas reinhardtii

Cited by 30 publications

References 53 publications

Organellar DNA Polymerases in Complex Plastid-Bearing Algae

Organellar DNA Polymerases in Complex Plastid-Bearing Algae

Intensive DNA Replication and Metabolism during the Lag Phase in Cyanobacteria

Chloroplast DNA Copy Number Changes during Plant Development in Organelle DNA Polymerase Mutants

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