Extensive methylation of chloroplast DNA by a nuclear gene mutation does not affect chloroplast gene transmission in chlamydomonas

doi:10.1016/0092-8674(82)90351-8

Cell

Volume 28, Issue 2, February 1982, Pages 335-343

https://doi.org/10.1016/0092-8674(82)90351-8 Get rights and content

Abstract

Based on analysis by high pressure liquid chromatography, greater than 35% of the cytosine residues in chloroplast DNA of vegetative cells were found to be methylated constitutively in the nuclear gene mutation (me-1) of Chlamydomonas reinhardtii, which has an otherwise wild-type phenotype. Digestion of chloroplast DNA from vegetative cells and gametes of this mutant with restriction endonucleases Hpa II and Msp I reveals that in the 5′CCGG3′ sequence, CpG is methylated extensively, whereas CpC is only methylated occasionally. Hae III (5′GGCC3′) digestion of the mutant chloroplast DNA also shows extensive methylation of the GpC sequence. In contrast to the results of Sager and colleagues, which show a correlation between methylation of chloroplast DNA and transmission of chloroplast genes in crosses, our results with crosses of the me-1 mutant suggest that extensive chloroplast DNA methylation may be insufficient to account for the pattern of inheritance of chloroplast genes in Chlamydomonas.

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Chloroplasts and mitochondria derive from free-living bacteria and possess their own genomes. Organellar genomes retain many of the essential genes for photosynthesis/respiration and organelle biogenesis. However, their replication, repair, and inheritance depend largely on nuclear gene products. Extant chloroplasts and mitochondria generally possess multicopy genomes localized within nucleoids, whose organization and regulation will provide critical information to elucidate how free-living bacteria evolved into eukaryotic organelles. This chapter reviews work on this subject in Chlamydomonas, including historical milestones and recent progress. Research highlights emphasize two topics: the dynamic regulation of chloroplast nucleoids during mitosis, and the uniparental inheritance of chloroplast DNA, involving selective degradation, during sexual reproduction.
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Citation Excerpt :
The methylation might protect mt+ cpDNA from digestion [44] or affect the relative rates of cpDNA replication in germinating zygotes [48]. On the other hand, other groups have reported that selective methylation of cpDNA is not necessarily correlated with uniparental inheritance of cpDNA [50,51]. The significance of selective methylation in uniparental inheritance of cpDNA is still controversial.
The mitochondrion is an organelle that has its own DNA (mtDNA). Mitochondria play essential roles in energy production and in various cellular processes such as metabolism and signal transduction. In most animals, including humans, although the sperm-derived paternal mitochondria enter the oocyte cytoplasm after fertilization, their mtDNA is never transmitted to the offspring. This pattern of mtDNA inheritance is well known as “maternal inheritance.” However, how the paternal mitochondria and mtDNA are eliminated from the cytoplasm of gametes or zygotes remains an enigma. Recently, a variety of mechanisms, including specific nuclease-dependent systems, ubiquitin–proteasome system, and autophagy have been shown to degrade the paternal mtDNA or the paternal mitochondria themselves in order to prevent paternal mtDNA transmission. In this review, we will address the current state of knowledge of the molecular mechanisms underlying the elimination of paternal mtDNA or mitochondrial structures for ensuring the maternal transmission of mtDNA.
Occurrence of DNA Methylation in Chloroplasts of the Suspension Cultured Cells from a Liverwort, Marchantia paleacea var. diptera
1994, Journal of Plant Physiology
Photosynthetically active chloroplasts were formed in Marchantia paleacea var. diptera cells grown under heterotrophic conditions in the dark. To obtain knowledge of a role of DNA methylation in the expression of chloroplast encoding genes, chloroplast and nuclear DNA were digested with methyl-sensitive and methyl-insensitive isoschizomers of EcoRII/BstNI, HpaII/MspI and MboI/Sau3AI. Digestion patterns showed that cytosine residues of a small amount of 5′ CCA(T)GG3′ sites of chloroplast DNA were methylated, while cytosine residues of a considerable amount of both 5' CCA(T)GG3' and 5' CCGG3' sites of nuclear DNA were methylated. HPLC analysis of base compositions indicated that 0.2% of cytosine was methylated in chloroplast DNA and 17% in nuclei. Digestion patterns in chloroplast DNA from photoautotrophically grown cells with those isoschizomer pairs were entirely the same as those from heterotrophically grown cells.
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DNA methylation may play a key role in some biological processes, as in DNA replication, transcription and recombination, gene expression, cell differentiation, and development. However, the experimental facts were elusive up to now.
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1990, Journal of Chromatography Library
Most DNAs contain minor amounts of 5-methyl cytosine (m⁵C), N⁶-methyl adenine (m⁶A), or N⁴-methyl cytosine (m⁴C). Any one or more of these can be found in most bacterial DNAs. Some lower eukaryotes have m⁵C, m⁶A, or both as a minor base in their genomes. In the DNA of all investigated vertebrates and higher plants, m⁵C, and only m⁵C, is the naturally occurring modified base. The levels and patterns of m⁵C in vertebrate genomes are tissue-specific. Some vertebrate DNA methylation has been linked to the regulation of gene transcription. As for m⁶A in the Escherichia coli genome, m⁵C in the DNA of eukaryotes may function in controlling DNA repair, replication, and rearrangements as well as in control of transcription. However, although bacterial DNA methylation is often involved in restriction-modification systems, there is no evidence for this function in the case of vertebrate DNA methylation. Vertebrate DNA methylation may, however, be an important determinant of chromatin structure. In addition to methylated bases present as minor DNA components, other modified bases are major components of certain bacteriophage genomes. These have one of their bases, usually a pyrimidine, largely or completely replaced by the modified derivative. The derivatives include glucosylated 5-hydroxy-methyl-cytosine, uracil, 5-hydroxymethyluracil, 5-(4-aminobutylaminomethyl)uracil, and glucosylated and glucuronic acid-1-phosphorylated 5-(4',5'-dihydroxypentyl)uracil.

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^∗: Present address: Department of Genetics, North Carolina State University, Raleigh, North Carolina 27607.

^†: Present address: Department of Biochemistry, Saint Louis University School of Medicine, Saint Louis, Missouri 63104.

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Cell

ArticleExtensive methylation of chloroplast DNA by a nuclear gene mutation does not affect chloroplast gene transmission in chlamydomonas

Abstract

Biochim. Biophys. Acta

J. Mol. Biol.

Prog. Nucl. Acid Res. Mol. Biol.

J. Mol. Biol.

Cell

Arch. Biochem. Biophys.

Ribosomal subunits affected by antibiotic resistance mutations at seven chloroplast loci in Chlamydomonas reinhardtii

Mol. Gen. Genet.

Evidence for persistence of chloroplast markers in the heteroplasmic state in Chlamydomonas reinhardtii

Current Genetics

Role of methylation in the modification and restriction of chloroplast DNA in Chlamydomonas

Replication of chloroplast DNA in Chlamydomonas reinhardi during vegetative cell cycle: its mode and regulation

Quantitative extraction of adenosine triphosphate from cultivable and host-grown microbes: calculation of adenosine triphosphate pools

Applied Microbiology

Induction of chromosomal and nonchromosomal mutations in Chlamydomonas reinhardi with N-methyl-N′-nitro-N-nitrosoguanidine

Genetics

Induced mutagenesis in dam− mutants of Escherichia coli: a role for 6-methyladenine residues in mutation avoidance

Mol. Gen. Genet.

[6N]methyl adenine in nuclear DNA of a eucaryote, Tetrahymena pyriformis

J. Cell Biol.

Site-specific methylation of chloroplast DNA in Chlamydomonas reinhardtii

J. Cell Biol.

Inheritance of chloroplast DNa in Chlamydomonas reinhardtii

Comparative study of DNA methylation in three unicellular eucaryotes

J. Bacteriol.

The roles of nitrate and ammonium in the regulation of the development of nitrate reductase in Chlamydomonas reinhardii

Planta

DNA modification mechanisms and gene activity during development

Science

Complementary specificity of restriction endonucleases of Diplococcus pneumoniae with respect to DNA methylation

J. Mol. Biol.

Gas-liquid chromatographic analysis for purine and pyrimidine bases in hydrolysates of nucleic acid

Clin. Chem.

The genetics and cytology of Chlamydomonas

Ann. Rev. Microbiol.

Article
Extensive methylation of chloroplast DNA by a nuclear gene mutation does not affect chloroplast gene transmission in chlamydomonas

Induced mutagenesis in dam⁻ mutants of Escherichia coli: a role for 6-methyladenine residues in mutation avoidance

[⁶N]methyl adenine in nuclear DNA of a eucaryote, Tetrahymena pyriformis