DNA transfer between internal organelles such as the nucleus, mitochondrion, and plastid is a well-known phenomenon in plant evolution, and DNA transfer from the plastid and mitochondrion to the nucleus, from the plastid to the mitochondrion, and from the nucleus to the mitochondrion has been well-documented in angiosperms. However, evidence of the transfer of mitochondrial DNA mtDNA to the plastid has only been found in three dicotyledons and one monocotyledon.
In the present study, we characterised and analysed two chloroplast cp genome sequences of Convallaria keiskei and Liriope spicata , and found that C. Interestingly, C. Further analyses revealed that mtDNA transfer only occurred in C. These findings indicate that the C. The engulfment of bacterial endosymbionts led to the development of eukaryotic cells, and the consequent gradual conversion of those bacteria into eukaryotic organelles such as the mitochondrion and chloroplast cp 1 , 2.
During this process, there was a significant transfer of cp and mitochondrial mt genes from the endosymbiont genomes into the nuclear genome of the host cell 3. Lateral and horizontal genetic material transfer between organisms and intracellular gene transfer IGT between genomes within organisms are common processes in both prokaryotes and eukaryotes rather than by vertical transfer through sexual reproduction 4 , 5 , 6 , 7 , 8.
In plants, the intracellular transfer of genetic material between the cp, mt and nuclear genomes is a common process. The IGT of plastid DNA to the mt and nuclear genomes and the transfer of plastid and mtDNA to the nuclear genome are well-documented and regular phenomena in the land plants 4 , 5 , 6 , 7 , 8. Also, previous studies reported that nuclear DNA has been transferred to mt genomes in the Fabaceae and Cucurbitaceae due to the presence of a permeable transition pore complex in the mitochondria 9 , Nevertheless, land plant plastomes are highly conserved and considered essentially immune to IGT, and it is thought that plant cp genomes do not accept the incorporation of foreign DNA because of the integrity of the plastid membrane 7 , 8 , However, four studies have documented mt gene transfer to plastomes.
In angiosperms, the mt pseudogene cox1 has been transferred into the plastome of Daucus carota 11 , 12 , 13 , rpl2 was transferred in the common milkweed 14 , a complete copy of ccmB was transferred in Anacardium occidentale 15 , and intergenic sequences were transferred in herbaceous bamboos In contrast, no evidence of nuclear DNA transfer into the plastid has been reported in any land plant.
In the present study, we characterised and analysed the complete cp genome sequences of two monocotyledon angiosperm plants, Convallaria keiskei Miq. We also analysed cp pseudogenes in the Asparagales in order to understand the evolutionary histories of these genes. Furthermore, we identified the transfer of mtDNA, including the rpl10 pseudogene, into the plastome of C.
Additional work confirmed that mtDNA transfer only occurred in the C. Finally, molecular evolutionary analyses suggested that C. To the best of our knowledge, this is the largest mtDNA segment that has been transferred into the cp genome of the monocotyledon C.
The plastid genomes of C. A total of 17 intron-containing genes 12 protein-coding genes and 5 tRNAs were present in both cp genomes. The predicted genes were divided into four categories based on their functions. The first category contained 34 genes, including rRNA and tRNA genes; the second category contained 48 genes that were associated with photosynthesis, including subunits of photosystem I and II, photosynthetic electron-transport-chain-component genes, the rubisco large subunit gene, and presumed NAD P H dehydrogenase subunit genes; the third category contained genes that were associated with transcription and translation; and the fourth category contained genes related to amino acids, fatty acids, other biosynthesis-related genes, and some genes with unknown functions Supplementary Table S2.
The cp genome size of C. The figure is not drawn to scale. Genes in the boundary regions were highly conserved, with small variations in the cp genomes of the Nolinoideae, except for P. The LSC region in P. However, in E. When compared with another subfamily of the Asparagaceae, the sizes of the LSC, SSC and IR regions of the Lomandroideae and Nolinoideae were extremely diverse, which reflects genome size variation and suggests that these plastomes are not highly conserved.
There was a close association between LSC length and genome size, whereas associations between SSC and IR lengths and genome size were highly variable. All of the photosynthetic- and transcriptional-related genes were present in the plastomes of both species, as in other Asparagales. However, some differences were observed in the protein-coding genes of the Asparagales. Specifically, large differences were found in the protein-coding and intergenic regions of the LSC in the plastomes of the Asparagales that contained a large number of pseudogenes, intron deletions and inversions Supplementary Table S3.
Most of these genes were related to transcription and translation, and are essential for land plants.
The pseudogenes included accD , infA , rpl23 , rpl32 , rps2 , rps16 , rps19 , and ycf1. The coding regions in the Nolinoideae plastomes of C. The protein-coding regions of the Nolinoideae were extracted and evaluated in order to identify divergent hotspots in the coding regions Supplementary Fig. Most of the protein-coding genes were highly conserved; however, minor divergences were detected. The infA gene had highly diverged due to the presence of a pseudogene in the Convallaria , Liriope and Nolina 18 cp genomes.
The cp gene infA of C. The functional infA gene sequence was highly variable in the Nolinoideae. The infA gene on the L. A similar pattern was observed in N. Phylogenetic analyses revealed that the loss of infA occurred independently in the Nolinoideae Fig. Previous studies have reported that the infA gene was independently lost from other monocotyledons, such as most of the Agavoideae, Allioideae, Aphyllanthoideae, Asphodeloideae, Brodiaeoideae, Lemnoideae, Lomandroideae, and other angiosperm lineages 17 , 18 , 19 , 20 , A comparison of the other plastome protein-coding genes of the Asparagales revealed that accD , rpl23 , rpl32 , rps2 , rps16 , rps19 and ycf1 are pseudogenes.
Comparative analysis revealed that all of the pseudogene or gene loss occurred independently in the Asparagales, except for rps16 in the Lomandroideae Fig. However, the cp genomes of several species of the Lomandroideae should be investigated in order to elucidate the evolution of rps Although several cp genes were deleted during evolution, these deletions are not related to the taxonomy of the Asparagales.
Taken together, these results suggest that most cp gene loss occurred independently across the Asparagales, as well as the angiosperms. Molecular phylogenetic tree of 27 Asparagales taxa based on 68 protein-coding genes in the chloroplast genome. The stability of each tree node was tested by bootstrap analysis with 1, replicates. Bootstrap values are indicated on the branches, and the branch length reflects the estimated number of substitutions per 1, sites.
Aloe vera and Xanthorrhoea preissii were set as the outgroups. In genome evolution studies, the ratio of non-synonymous dN to synonymous dS substitutions is an important indicator The majority of genes in the Nolinoideae genomes had ratios of less than 1. Although a missense mutation occurred in these genes, they are under positive selection in Nolinoideae cp genomes, possibly by adapting to changing ecological conditions. One-third of plastid genes, including self-replication- and photosynthesis-related genes, evolved under positive selection in the Poaceae In contrast, in the Nolinoideae, the substitution ratios were less than one for most of the photosynthetic-related genes, except for cemA , rbcL and psbK , which are transcription and translation genes that are more highly conserved than other genes in cp genomes because of strong functional constraints.
Ratio of non-synonymous dN to synonymous dS substitutions of 68 protein-coding genes in the Nolinoideae. Basal eudicots encode AUG as the initiation codon for most protein-coding genes, but the Convallaria and Liriope cp genomes encode an alternative starting codon ACG for rpl2. A similar type of codon was observed in all of the Asparagales cp genomes. An analysis of the codon usage patterns of 68 unique cp protein-coding genes in 27 Asparagales taxa revealed that , codons were present in the protein-coding genes.
Figure 5 is a heatmap of codon usage in the Asparagales. Similar results have been obtained in many other land plant and algal lineages The high RSCU values of the codons indicate amino acid functions or peptide structures that inhibit transcriptional errors in cp genomes. Codon distributions of chloroplast protein-coding genes in the Asparagales. Hierarchical clustering average linkage method was performed for the codon patterns x-axis.
To elucidate the phylogenetic relationships of the Asparagales, 68 cp protein-coding genes shared by 27 genomes were investigated. The phylogenetic tree was divided into three groups: the Xanthorrhoeaceae, Amaryllidaceae, and Asparagaceae Fig. The Xanthorrhoeaceae is basal to the rest of the Asparagales. Two major clades formed in the Asparagaceae, with the Lomandroideae, Asparagoideae and Nolinoideae in one clade and the Agavoideae, Aphyllanthoideae and Brodiaeoideae in the other.
This weak BS value may have been caused by indels and nucleotide differences in the protein-coding genes of their respective cp genomes. The aim was to estimate divergence time for the Nolinoideae, but due to a lack of calibration points, we included other species of Asparagales. Divergence time was estimated using previous data of the Asparagales, which were similar to those obtained in the present study.
In addition, the species used in both the maximum likelihood phylogenetic tree and the divergence analysis were the same. Among the Asparagales, the Xanthorrhoeaceae basal group Aloe vera and Xanthorrhoea preissii diverged In the Asparagaceae, the Asparagoideae A. Chronogram results from a BEAST analysis revealed that all of the speciation events within Nolinoideae occurred from Polygonatum diverged from the ancestor of all other members of the Nolinoideae at Both of them encodes for proteins and RNAs vital to their functions.
Nuclear DNAs are compacted into chromatin structures through histones. During mitosis and meiosis, mitochondria and chloroplasts randomly segregate. Thus, their genetic material segregates randomly as well into new daughter cells. The pattern of inheritance involving cpDNA does not follow the Mendelian pattern of inheritance. Rather, certain traits are inconsistent with the Mendelian laws. In , he noticed that the same plant had a mixture of leaf colors, i.
Pollinating the flower of one leaf color e. DNA replication is a process whereby the original parent strands of DNA in the double helix are separated and each one is copied to produce a new daughter strand. DNA carries the genetic information that codes for a particular protein. Rubisco is the major protein component of the chloroplast stroma.
It is the enzyme that catalyzes the addition of CO 2 to ribulose-1,5-bisphosphate during the Calvin cycle. Supplementary Table 2. Allen, J. Why chloroplasts and mitochondria retain their own genomes and genetic systems: colocation for redox regulation of gene expression.
Boffey, S. Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol. Christensen, A. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons.
Plant Cell 17, — Cupp, J. Minireview: DNA replication in plant mitochondria. Mitochondrion 19, — Emanuelsson, O. Locating proteins in the cell using TargetP, SignalP and related tools. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. Grevich, J. Chloroplast genetic engineering: recent advances and future perspectives. Critical Rev. Plant Sci. Gualberto, J. The plant mitochondrial genome: dynamics and maintenance.
Biochimie , — Hori, A. Reactive oxygen species regulate DNA copy number in isolated yeast mitochondria by triggering recombination-mediated replication. Acids Res. Kabeya, Y. Chloroplast DNA replication is regulated by the redox state independently of chloroplast division in Chlamydomonas reinhardtii. Kimura, S. Kolodner, R. Chloroplast DNA from higher plants replicates by both the Cairns and rolling circle mechanism.
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Kunnimalaiyaan, M. Chloroplast DNA replication: mechanism, enzymes and replication origins. Plant Biochem. Liere, K. Biswal, K. Krupinska, and U. Biswal Dordrecht: Springer , — CrossRef Full Text. Maliga, P. Plastid biotechnology: food, fuel, and medicine for the 21 st century. Minas, K. FEMS Microbiol. Mori, Y. Plastid DNA polymerases from higher plants, Arabidopsis thaliana.
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Nielsen, B. Mechanisms for maintenance, replication and repair of the chloroplast genome in plants. Oldenburg, D. Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms.
Ono, Y. Plant Cell Physiol. Palmer, J. On the other hand, abundant cpDNAs are reported to undergo degradation during leaf senescence of annual plants or during leaf fall in trees Fulgosi et al. Cytological observations of cpDNA degradation during leaf senescence have been extensively studied by the Kuroiwa group Inada et al.
Their results indicate that organelle DNA degradation is linked to nutrient recycling, although it remains unclear whether degradation proceeds nucleolytically or is accompanied by other hydrolytic degradation processes.
In an earlier study Matsushima et al. One of the mutants isolated, named defective in pollen organelle dna degradation 1 dpd1 , resulted in the identification of the DPD1 exonuclease.
The detailed analysis of DPD1 fulfilled the observed characteristics of organelle DNA degradation: DPD1 is targeted to both chloroplasts and mitochondria; is well conserved in flowering plants producing pollen ; is up-regulated in pollen; and exhibits exonuclease activity.
While further experimental evidence is needed to support this hypothesis, an in silico survey of mRNA accumulation in various tissues clearly indicated that DPD1 transcript accumulates substantially not only in pollen but also in senescing leaves Tang and Sakamoto , Sakamoto and Takami While the up-regulation of DPD1 in pollen and senescing leaves explained previous cytological observations of cpDNA degradation, it raised other issues for future studies to address.
For example, the presence of other factors implicated in DNA degradation should be considered, such as endonucleolytic activity, which ought to exist to assist DPD1 in degrading cpDNA from the 3' ends. Intriguingly, cpDNAs are rich in nicked or single-stranded forms, as indicated by previous work from the Bendich group reviewed by Bendich , Oldenburg and Bendich , and due to the proposed mode of DNA replication through repeated sequences and R-loops Yang et al. Given such heterogeneous populations, it is likely that DPD1 is sufficient to degrade a substantial portion of cpDNA and also mtDNA without the need for additional factors.
Discrepancies in the amounts of cpDNA in mature leaves are likely to be explained by DPD1 activity, which may vary even within leaf tissues. Moreover, the fact that cpDNA tends to accumulate DNA damage and detrimental rearrangements, leading to chloroplast dysfunction Nielsen et al. Further studies are needed to clarify this possibility. Nucleoids alter their morphology depending on the developmental status of chloroplasts; a process that represents their principal requirement in transcription and translation.
In contrast, how the change in cpDNA copy number is associated with chloroplast development remains elusive. Proteome analysis is unable to confirm the presence of DPD1 in nucleoids, so a tight control of DNA degradation is plausible.
Thus the relationship between nucleoid structure and the DPD1-mediated degradation mechanism should be investigated in the future. The most fundamental question that remains to be answered is the physiological significance of cpDNA degradation. Chloroplasts also comprise a significant population of nucleotide pools, as represented largely by chloroplast rRNAs Stigter and Plaxton Given that exonucleolytic degradation of cpDNA releases pools of nucleotide, sugar and phosphate, DPD1-mediated degradation of organelle DNA could benefit plant growth, particularly under conditions where external nutrients are limited.
Thus, the rescue of nucleic acids in chloroplasts might be one reason for cpDNA degradation in flowering plants. Supporting this rescue function, we have shown that de novo synthesis of nucleotides is associated with organelle DNA degradation Tang et al.
In conclusion, the emergence of DPD1 is confined to the flowering plants, where ptDNA degradation is beneficial for sustaining pollen survival, and possibly required later during leaf senescence to provide a nutrient reservoir for the plant. Although a similar degradation mechanism remains to be identified in green algae, such a reservoir function has been postulated in Chlamydomonas Sears and VanWinkle-Swift Thus the relationship between nutrient supply and cpDNA dynamics will certainly be an interesting area of research for future studies.
We apologize to those authors whose works could not be discussed in this article due to space limitations; priority was instead given to discussing articles that covered topics related to cpDNA dynamics. Arimura S. Plant Physiol. Google Scholar. Bendich A. Plant Cell 16 : — Carrie C. Plant J. Chan K. Plant Biol. Chi W. Corriveau J. Cupp J. Desveaux D. Cell 6 : — Diray-Arce J. BMC Plant Biol. Dyall S. Science : — Foyer C. B: Biol. Fujie M. Planta : — Fulgosi H.
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Edited by Wise R. Springer , Dordrecht, The Netherlands. Google Preview. Kuroiwa T. Plant Res. Lepage E. Maier R.
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