Why chloroplasts and mitochondria have dna

In yeast mitochondria the nucleoid protein mtTBP has been shown to bind to single-stranded DNA at the telomeres and has been proposed to function in the replication, stabilization, and maintenance of linear mtDNA molecules Tomaska et al. We propose that in plastids, Whirlies bind to and protect the ends of ptDNA, as well as mediating the attachment of nucleoids to membranes.

If the Whirly interaction with the membrane is responsive to the plastid redox state, then dissociation of Whirlies from the membrane and from the ptDNA ends may be triggered in photosynthetically active chloroplasts, thus releasing DNA from the nucleoid and exposing the ends to nuclease activity. DNA damage and repair are typically studied by treating plants, animals, or their cultured cells with agents known to cause DNA damage irradiation or peroxide, for example and then comparing results from the treated and untreated samples Yakes and Van Houten, ; Parent et al.

It also reports the net result of damage plus repair. Another approach is to quantify the amount of transcripts, protein, or enzymatic activity from DNA-repair genes, which provides information concerning the capacity to repair damage, rather than the act of repair itself. For plants, some types of orgDNA lesions and repair pathways have been identified Marechal and Brisson, ; Balestrazzi et al.

A common approach to study replication in the absence of repair, and vice versa , is to obtain mutants in one or the other component of DNA maintenance.

In Arabidopsis , mutation in the nucleus-encoded, plastid-targeted recA1 cprecA gene led to no alteration in leaf morphology for three generations and only a rather subtle change in leaf variegation yellow and white sectors in the following 4 to 8 generations—a surprisingly mild defect considering that RecA is the most highly conserved recombination protein Rowan et al.

Similarly, Arabidopsis single mutants of why1 and why3 and the double mutant reca1polIb resulted in no phenotypic alteration, and it was only in the why1why3 double mutant and triple mutants why1why3polb and why1why3reca1 that a defect in leaf morphology was evident Marechal et al.

Thus, it appears that Arabidopsis employs several biochemical pathways to maintain sufficient levels of high-integrity ptDNA for chloroplast biogenesis.

There was, however, a decrease in the amount of ptDNA in the recA1 , polIa , and polIb single mutants compared to wild-type young seedlings Rowan et al. These mutations may also have disrupted the normal replication process by inhibiting precise recombination at defined regions adjacent to the oris that leads to branched multigenomic molecules because these proteins likely function in both replication and repair.

Since both photosynthesis and respiration produce ROS as unavoidable by-products, it may be expected that damage to orgDNA would increase as maize leaves develop.

The amount of damage measured as impediments to DNA polymerase per 10 kb of orgDNA was lowest at the base of the stalk and increased during leaf development in the dark as well as after transfer of dark-grown seedlings to light Kumar et al.

To summarize, although the capacity to repair damaged orgDNA has long been known for plants and animals, only recently—and for only one plant species—has repairable damage of orgDNA been quantified under normal development without the addition of stress or genotoxic agents. Light affects both damage and levels of functional DNA in both plastids and mitochondria, even though mitochondria have no known photoreceptors.

Although this conclusion likely applies to Arabidopsis Rowan and Bendich, , we currently lack long-PCR and in vitro repair assay data in order to evaluate the quantity and quality of orgDNA molecules as proplastids and their mitochondrial counterparts mature to the organelles found in the green leaf. One possibility is that repair in maize occurs only in the meristem, so that unrepaired orgDNA in the green chloroplasts is degraded: orgDNA abandonment.

During proplastid-to-chloroplast development, the DNA level per plastid first increases and then decreases, although the magnitude of the decline varies among species. For example, ptDNA increases later and remains high longer for both Arabidopsis and tobacco than maize Figure 4.

In mature tobacco leaves, nearly all cells contain chloroplasts with DAPI-fluorescent nucleoids Shaver et al. Furthermore, the genomic monomer and oligomers are prominent in PFGE of ptDNA from mature leaves of many dicots, but in maize even the monomer is barely detectable Lilly et al.

Figure 4. Schematic representation of changes in the amount of ptDNA per plastid during development in three plant species. Increase in ptDNA amount due to ptDNA replication occurs very early in development in maize red line , followed by a rapid decline.

For tobacco gray line , ptDNA increases more gradually and the decline is less severe. The Roman numerals indicate stages of leaf development.

Reprinted from Rowan and Bendich, In dicots, such as Arabidopsis and tobacco, cell division is not restricted to the apical meristem, but continues along a base-to-tip gradient in the expanding leaf Donnelly et al. Except for the meristem, which is enclosed in the bud and shielded from light, cell development and elongation occur in the light. Thus in grasses, there is a prolonged etioplast-like developmental stage in the expanding leaf followed by an abrupt transition to a green chloroplast as the leaf tip emerges from the sheath, whereas photosynthetic chloroplasts are present throughout development of a dicot leaf.

The ROS produced during photosynthesis would necessitate greater ptDNA-protective measures in the expanding dicot leaf, which could persist at a reduced level in mature leaves.

In contrast, little ptDNA protection is evidently provided in green chloroplasts of maize, as indicated by the rapid ptDNA decline upon light exposure Zheng et al.

There are also differences in DNA maintenance proteins. In maize only one Whirly protein, Why1, has been reported Marechal et al. Therefore, greening during the etioplast-to-chloroplast transition in maize would lead to loss of ptDNA from ROS-mediated damage without repair.

The ptDNA in the dicot leaf must be kept in good repair—and at substantial cost—during the period of ptDNA replication, which is concurrent with photosynthesis and chloroplast expansion. In grasses, by contrast, etioplast expansion to a size equivalent to a green chloroplast, ptDNA replication, and, critically, production of all the ptDNA-encoded mRNAs required for photosynthesis during the coming plant growth season, all proceed without the DNA-damaging ROS by-product of photosynthesis.

Replacement of the ancestral apical meristem proplastid-to-chloroplast progression in dicots with a basal meristem proplastid-to-etioplast-to-chloroplast transition in grasses may have been advantageous.

In mid-latitudes 55—70 million years ago, selective pressures included seasonally dry climates, wildfires, and herbivory Bond and Scott, A ground-level basal meristem may provide greater tolerance to drought-stress and defoliation by mammals. By abandoning ptDNA in mature leaves, grasses may realize a cost saving by not repairing DNA damaged by increased ROS from drought-stress and not investing in ptDNA maintenance in mature leaves that would be lost to fire or herbivory.

We have a relatively good understanding of the replication and repair apparatus that maintains nuclear DNA at a constant, diploid level throughout development. By comparison, there is disagreement concerning the maintenance of orgDNA in the same cells. Rather than infer the properties of orgDNA molecules from enzyme requirements and indirect methods like RNA analysis, the quality, quantity and stability of orgDNA molecules themselves should be investigated during development from meristem to green leaf.

The data showing the demise of orgDNA during leaf maturation have not been well received by some, and the controversy has been presented recently Golczyk et al. There are four main reasons for skepticism. First, some proteins, especially the product of the psbA gene D1 , turn over very rapidly and must be continuously replaced for photosynthesis to occur.

Thus, either there must be a functional psbA gene in the green chloroplast to supply the mRNA for ongoing production of D1 protein during photosynthesis or the mRNA for D1 is extremely stable.

The third reason is that an in vitro run-on transcription assay shows that ptDNA is present in the chloroplasts isolated from green leaves of barley Emanuel et al. In this assay, radiolabeled UTP is incorporated into the growing RNA chain that had been initiated before the leaves were harvested. Furthermore, transcripts from highly-fragmented ptDNA might not benefit the cell from their coding potential, but instead represent the residuum from transcription-coupled repair, a proposed global surveyor of DNA damage Epshtein et al.

The suggestion has also been made that the data indicating the demise of orgDNA are due to methodological artifacts Golczyk et al. We conclude that during proplastid-to-chloroplast development, the ptDNA level initially increases to supply the gene products needed for photosynthesis.

After chloroplast maturation, excess copies are no longer needed, degraded, and the nucleotides recycled. The fourth reason is that cytological images of DAPI-stained nucleoids indicate the persistence of some ptDNA in expanded green leaves of several plants Golczyk et al. These data, however, are not quantitative, do not reflect the quality of the ptDNA molecules, and do not report the fraction of DAPI-positive chloroplasts among chloroplasts chosen at random for analysis.

The genome copy number per individual chloroplast chosen at random before quantitative analysis of DAPI fluorescence varied from 0 to for the first green leaf of maize Zheng et al. Thus the detection of DAPI-positive nucleoids does not necessarily indicate that the nucleoids contain ptDNA molecules of high quality. The amount and degree of molecular integrity of DNA present in a particular tissue are determined by replication, repair, and stability of the DNA.

For the diploid nucleus, these processes are governed by checkpoint control in such a way as to result in a constant amount of stable, intact chromosomal DNA molecules throughout development, regardless of the physiological activities of the cells.

In other words, orgDNA—but usually not nuclear DNA—can be abandoned in somatic cells as part of the normal developmental process. The advantage of DNA abandonment leading to DNA-repair cost savings and embryonic development in plants and animals has been discussed previously Bendich, b , Although DNA could not be abandoned in the bacterial ancestors of plastids and mitochondria, orgDNA abandonment in leaves has evidently been advantageous, especially for grasses.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

This work was funded by the Junat Fund a private charitable fund. The authors thank Beth A. Rowan for critical reading of this manuscript. Alexeyev, M. The maintenance of mitochondrial DNA integrity—critical analysis and update. Cold Spring Harb. Alverson, A. Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo Cucurbitaceae. Balestrazzi, A. Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity.

Plant Cell Rep. Baumgartner, B. Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol. Bendich, A. Why do chloroplasts and mitochondria contain so many copies of their genome?

Bioessays 6, — Moving pictures of DNA released upon lysis from bacteria, chloroplasts, and mitochondria. Protoplasma , — Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. The form of chromosomal DNA molecules in bacterial cells. Biochimie 83, — The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts.

Bioessays 29, — The end of the circle for yeast mitochondrial DNA. DNA abandonment and the mechanisms of uniparental inheritance of mitochondria and chloroplasts. Chromosome Res. Moving pictures and pulsed-field gel electrophoresis show linear DNA molecules from chloroplasts and mitochondria.

Boesch, P. DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Acta , — Bond, W. Fire and the spread of flowering plants in the Cretaceous. New Phytol. Cairns, J. The chromosome of Escherichia coli. Cappadocia, L. Plant Cell 22, — A conserved lysine residue of plant Whirly proteins is necessary for higher order protein assembly and protection against DNA damage. Nucleic Acids Res.

Carrie, C. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Chaconas, G. Structure, function, and evolution of linear replicons in Borrelia. Chang, C. Christin, P. Molecular dating, evolutionary rates, and the age of the grasses.

Coleman, A. Cell Biol. Cox, M. Motoring along with the bacterial RecA protein. Cupp, J. Minireview: DNA replication in plant mitochondria. Mitochondrion 19 Pt B, — Dai, H. Structural and functional characterizations of mung bean mitochondrial nucleoids.

Dickey, T. Single-stranded DNA-binding proteins: multiple domains for multiple functions. Structure 21, — Diray-Arce, J. BMC Plant Biol. Donnelly, P. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Emanuel, C. Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J. Epshtein, V. Nature , — Foyer, C.

Fujie, M. Studies on the behavior of organelles and their nucleoids in the root apical meristem of Arabidopsis thaliana L. Planta , — Behavior of organelles and their nucleoids in the shoot apical meristem during leaf development in Arabidopsis thaliana L.

Fukui, K. Gilkerson, R. The mitochondrial nucleoid: integrating mitochondrial DNA into cellular homeostasis. Golczyk, H. Chloroplast DNA in mature and senescing leaves: a reappraisal.

Plant Cell 26, — Gutman, B. Evidence for base excision repair of oxidative DNA damage in chloroplasts of Arabidopsis thaliana. Hashimoto, H. DNA levels in dividing and developing plastids in expanding primary leaves of Avena sativa. Heinhorst, S. DNA replication in chloroplasts. Cell Sci. Google Scholar. Kabeya, Y. The YlmG protein has a conserved function related to the distribution of nucleoids in chloroplasts and cyanobacteria. Woo, J. Zong, Y. Precise base editing in rice, wheat and maize with a Cas9—cytidine deaminase fusion.

Shimatani, Z. Kang, B. Precision genome engineering through adenine base editing in plants. Plants 4 , — Howad, W. Cell type-specific loss of atp6 RNA editing in cytoplasmic male sterile Sorghum bicolor.

USA 94 , — Fromm, H. Plant Mol. Lee, H. Millen, R. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13 , — Lee, D. Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20 , — Arimura, S. USA 99 , — Lee, S. Mitochondrial targeting of the Arabidopsis F1-ATPase gamma-subunit via multiple compensatory and synergistic presequence motifs.

Plant Cell 24 , — Lelivelt, C. Stable plastid transformation in lettuce Lactuca sativa L. Pelletier, G. Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Park, J. Cas-analyzer: an online tool for assessing genome editing results using NGS data.

Bioinformatics 33 , — Download references. This work was supported by grants from the Institute for Basic Science no. You can also search for this author in PubMed Google Scholar. Correspondence to Jin-Soo Kim. All the other authors declare no competing interests. Reprints and Permissions. Kang, BC. Chloroplast and mitochondrial DNA editing in plants.

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Provided by the Springer Nature SharedIt content-sharing initiative. Nature Plants The proposal advanced here is that co-location of chloroplast and mitochondrial genes with their gene products is required for rapid and direct regulatory coupling. Redox control of gene expression is suggested as the common feature of those chloroplast and mitochondrial proteins that are encoded in situ.

Recent evidence is consistent with this hypothesis, and its underlying assumptions and predictions are described. These references are in PubMed. This may not be the complete list of references from this article. National Center for Biotechnology Information , U. Journal List Comp Funct Genomics v. Comp Funct Genomics. John F. Author information Article notes Copyright and License information Disclaimer.

Allen, Email: es. Corresponding author. Received Sep 17; Accepted Nov This article has been cited by other articles in PMC. Abstract Chloroplasts and mitochondria originated as bacterial symbionts. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants.

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