Plant Organelle DNA Maintenance

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Molecular Biology".

Deadline for manuscript submissions: closed (31 January 2020) | Viewed by 37373

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Special Issue Editors


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Guest Editor
Department of Microbiology & Molecular Biology, Brigham Young University, Provo, UT 84602, USA
Interests: plant molecular biology; DNA replication and recombination; plant mitochondrial and chloroplast genomes; salt-tolerant microbiomes
Agricultural Biotechnology Division, National Institute for Biotechnology & Genetic Engineering (NIBGE), 38000 Faisalabad, Pakistan
Interests: chloroplast biotechnology; biopharming; stress physiology; improving photosynthesis

Special Issue Information

Dear Colleagues,

In addition to the nuclear genome, plant cells also contain DNA in two of their organelles—plastids and mitochondria. These double-membrane-bound organelles are considered to have originated through endosymbiosis. Over the course of evolution, the modern-day plant organelle genomes have considerably shrunk compared to their progenitors, as genes move from the organelles to the nuclear genomes. This provides additional control points for the nucleus over plant and organelle development, physiology, and maintenance. Consequently, the products of genes that have migrated to the nucleus have to be imported into their corresponding organelle destination, which has resulted in the evolution of a sophisticated signaling network between the nucleus and the organelles for synthesis and quality control. Both the plastids and the mitochondria house important biochemical reactions, namely, photosynthesis and respiration, respectively. In addition to photosynthesis and respiration, these organelles play a central role in various metabolic reactions, such as amino acid synthesis, sucrose metabolism, nitrogen assimilation, sulphur metabolism, steroid synthesis, and apoptosis. Both the organelles and their genomes are present in high copy number. Depending upon the plant age and tissue type, their number, morphology, and genomic content vary considerably during cell division as well as in response to different stresses, reflecting the diversity of organelles’ functions. For example, the DNA copy number in plastids and mitochondria can reach very high levels in rapidly growing plant tissues, such as young leaves for plastid DNA and shoot and root meristems for mitochondrial DNA. Likewise, the DNA in both organelles is degraded in aging leaves, and the components are recycled. The mechanisms that control copy number and DNA replication are poorly understood. Displacement loop replication origins have been mapped and studied in plant chloroplast DNA, and the major proteins involved in replication have been identified. The situation is more complex for plant mitochondrial genomes, which appear to replicate by a recombination-dependent mechanism without any known origin of replication. The link between the metabolic needs of a cell and the capacity of organelles to fulfil this demand is thought to act as a selective force on the number of organelles in a cell. Many questions, including why the DNA and the organelles themselves exist in high copy number and how the organelles’ genomes are maintained through different developmental stages, remain yet to be fully understood.

This Special Issue of Plants is poised to address these questions. The issue focuses on organelle DNA dynamics in plants, with particular emphasis on fluctuations in organelle DNA, mechanisms to maintain DNA copy number, and its degradation.

Prof. Brent L. Nielsen
Dr. Niaz Ahmad
Guest Editors

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Keywords

  • Plant mitochondrial genomes
  • chloroplast genomes
  • recombination-dependent DNA replication
  • organelle DNA maintenance

Published Papers (9 papers)

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Editorial

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5 pages, 194 KiB  
Editorial
Plant Organelle DNA Maintenance
by Niaz Ahmad and Brent L. Nielsen
Plants 2020, 9(6), 683; https://doi.org/10.3390/plants9060683 - 28 May 2020
Cited by 5 | Viewed by 2210
Abstract
Plant cells contain two double membrane bound organelles, plastids and mitochondria, that contain their own genomes. There is a very large variation in the sizes of mitochondrial genomes in higher plants, while the plastid genome remains relatively uniform across different species. One of [...] Read more.
Plant cells contain two double membrane bound organelles, plastids and mitochondria, that contain their own genomes. There is a very large variation in the sizes of mitochondrial genomes in higher plants, while the plastid genome remains relatively uniform across different species. One of the curious features of the organelle DNA is that it exists in a high copy number per mitochondria or chloroplast, which varies greatly in different tissues during plant development. The variations in copy number, morphology and genomic content reflect the diversity in organelle functions. The link between the metabolic needs of a cell and the capacity of mitochondria and chloroplasts to fulfill this demand is thought to act as a selective force on the number of organelles and genome copies per organelle. However, it is not yet clear how the activities of mitochondria and chloroplasts are coordinated in response to cellular and environmental cues. The relationship between genome copy number variation and the mechanism(s) by which the genomes are maintained through different developmental stages are yet to be fully understood. This Special Issue has several contributions that address current knowledge of higher plant organelle DNA. Here we briefly introduce these articles that discuss the importance of different aspects of the organelle genome in higher plants. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)

Research

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16 pages, 4175 KiB  
Article
The First Plastid Genome of the Holoparasitic Genus Prosopanche (Hydnoraceae)
by Matthias Jost, Julia Naumann, Nicolás Rocamundi, Andrea A. Cocucci and Stefan Wanke
Plants 2020, 9(3), 306; https://doi.org/10.3390/plants9030306 - 1 Mar 2020
Cited by 15 | Viewed by 3539
Abstract
Plastomes of parasitic and mycoheterotrophic plants show different degrees of reduction depending on the plants’ level of heterotrophy and host dependence in comparison to photoautotrophic sister species, and the amount of time since heterotrophic dependence was established. In all but the most recent [...] Read more.
Plastomes of parasitic and mycoheterotrophic plants show different degrees of reduction depending on the plants’ level of heterotrophy and host dependence in comparison to photoautotrophic sister species, and the amount of time since heterotrophic dependence was established. In all but the most recent heterotrophic lineages, this reduction involves substantial decrease in genome size and gene content and sometimes alterations of genome structure. Here, we present the first plastid genome of the holoparasitic genus Prosopanche, which shows clear signs of functionality. The plastome of Prosopanche americana has a length of 28,191 bp and contains only 24 unique genes, i.e., 14 ribosomal protein genes, four ribosomal RNA genes, five genes coding for tRNAs and three genes with other or unknown function (accD, ycf1, ycf2). The inverted repeat has been lost. Despite the split of Prosopanche and Hydnora about 54 MYA ago, the level of genome reduction is strikingly congruent between the two holoparasites although highly dissimilar nucleotide sequences are observed. Our results lead to two possible evolutionary scenarios that will be tested in the future with a larger sampling: 1) a Hydnoraceae plastome, similar to those of Hydnora and Prosopanche today, existed already in the most recent common ancestor and has not changed much with respect to gene content and structure, or 2) the genome similarities we observe today are the result of two independent evolutionary trajectories leading to almost the same endpoint. The first hypothesis would be most parsimonious whereas the second would point to taxon dependent essential gene sets for plants released from photosynthetic constraints. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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18 pages, 1158 KiB  
Article
Mitochondrial DNA Repair in an Arabidopsis thaliana Uracil N-Glycosylase Mutant
by Emily Wynn, Emma Purfeerst and Alan Christensen
Plants 2020, 9(2), 261; https://doi.org/10.3390/plants9020261 - 18 Feb 2020
Cited by 8 | Viewed by 3164
Abstract
Substitution rates in plant mitochondrial genes are extremely low, indicating strong selective pressure as well as efficient repair. Plant mitochondria possess base excision repair pathways; however, many repair pathways such as nucleotide excision repair and mismatch repair appear to be absent. In the [...] Read more.
Substitution rates in plant mitochondrial genes are extremely low, indicating strong selective pressure as well as efficient repair. Plant mitochondria possess base excision repair pathways; however, many repair pathways such as nucleotide excision repair and mismatch repair appear to be absent. In the absence of these pathways, many DNA lesions must be repaired by a different mechanism. To test the hypothesis that double-strand break repair (DSBR) is that mechanism, we maintained independent self-crossing lineages of plants deficient in uracil-N-glycosylase (UNG) for 11 generations to determine the repair outcomes when that pathway is missing. Surprisingly, no single nucleotide polymorphisms (SNPs) were fixed in any line in generation 11. The pattern of heteroplasmic SNPs was also unaltered through 11 generations. When the rate of cytosine deamination was increased by mitochondrial expression of the cytosine deaminase APOBEC3G, there was an increase in heteroplasmic SNPs but only in mature leaves. Clearly, DNA maintenance in reproductive meristem mitochondria is very effective in the absence of UNG while mitochondrial genomes in differentiated tissue are maintained through a different mechanism or not at all. Several genes involved in DSBR are upregulated in the absence of UNG, indicating that double-strand break repair is a general system of repair in plant mitochondria. It is important to note that the developmental stage of tissues is critically important for these types of experiments. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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16 pages, 30654 KiB  
Article
New Insights on Lilium Phylogeny Based on a Comparative Phylogenomic Study Using Complete Plastome Sequences
by Hyoung Tae Kim, Ki-Byung Lim and Jung Sung Kim
Plants 2019, 8(12), 547; https://doi.org/10.3390/plants8120547 - 27 Nov 2019
Cited by 15 | Viewed by 3547
Abstract
The genus Lilium L. is widely distributed in the cold and temperate regions of the Northern Hemisphere and is one of the most valuable plant groups in the world. Regarding the classification of the genus Lilium, Comber’s sectional classification, based on the [...] Read more.
The genus Lilium L. is widely distributed in the cold and temperate regions of the Northern Hemisphere and is one of the most valuable plant groups in the world. Regarding the classification of the genus Lilium, Comber’s sectional classification, based on the natural characteristics, has been primarily used to recognize species and circumscribe the sections within the genus. Although molecular phylogenetic approaches have been attempted using different markers to elucidate their phylogenetic relationships, there still are unresolved clades within the genus. In this study, we constructed the species tree for the genus using 28 Lilium species plastomes, including three currently determined species (L. candidum, L. formosanum, and L. leichtlinii var. maximowiczii). We also sought to verify Comber’s classification and to evaluate all loci for phylogenetic molecular markers. Based on the results, the genus was divided into two major lineages, group A and B, consisting of eastern Asia + Europe species and Hengduan Mountains + North America species, respectively. Sectional relationships revealed that the ancestor Martagon diverged from Sinomartagon species and that Pseudolirium and Leucolirion are polyphyletic. Out of all loci in that Lilium plastome, ycf1, trnF-ndhJ, and trnT-psbD regions are suggested as evaluated markers with high coincidence with the species tree. We also discussed the biogeographical diversification and long-distance dispersal event of the genus. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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13 pages, 1732 KiB  
Article
Organization Features of the Mitochondrial Genome of Sunflower (Helianthus annuus L.) with ANN2-Type Male-Sterile Cytoplasm
by Maksim S. Makarenko, Alexander V. Usatov, Tatiana V. Tatarinova, Kirill V. Azarin, Maria D. Logacheva, Vera A. Gavrilova, Igor V. Kornienko and Renate Horn
Plants 2019, 8(11), 439; https://doi.org/10.3390/plants8110439 - 23 Oct 2019
Cited by 8 | Viewed by 3713
Abstract
This study provides insights into the flexibility of the mitochondrial genome in sunflower (Helianthus annuus L.) as well as into the causes of ANN2-type cytoplasmic male sterility (CMS). De novo assembly of the mitochondrial genome of male-sterile HA89(ANN2) sunflower line was performed [...] Read more.
This study provides insights into the flexibility of the mitochondrial genome in sunflower (Helianthus annuus L.) as well as into the causes of ANN2-type cytoplasmic male sterility (CMS). De novo assembly of the mitochondrial genome of male-sterile HA89(ANN2) sunflower line was performed using high-throughput sequencing technologies. Analysis of CMS ANN2 mitochondrial DNA sequence revealed the following reorganization events: twelve rearrangements, seven insertions, and nine deletions. Comparisons of coding sequences from the male-sterile line with the male-fertile line identified a deletion of orf777 and seven new transcriptionally active open reading frames (ORFs): orf324, orf327, orf345, orf558, orf891, orf933, orf1197. Three of these ORFs represent chimeric genes involving atp6 (orf1197), cox2 (orf558), and nad6 (orf891). In addition, orf558, orf891, orf1197, as well as orf933, encode proteins containing membrane domain(s), making them the most likely candidate genes for CMS development in ANN2. Although the investigated CMS phenotype may be caused by simultaneous action of several candidate genes, we assume that orf1197 plays a major role in developing male sterility in ANN2. Comparative analysis of mitogenome organization in sunflower lines representing different CMS sources also allowed identification of reorganization hot spots in the mitochondrial genome of sunflower. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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16 pages, 3033 KiB  
Article
De Novo Assembly Discovered Novel Structures in Genome of Plastids and Revealed Divergent Inverted Repeats in Mammillaria (Cactaceae, Caryophyllales)
by Sofía Solórzano, Delil A. Chincoya, Alejandro Sanchez-Flores, Karel Estrada, Clara E. Díaz-Velásquez, Antonio González-Rodríguez, Felipe Vaca-Paniagua, Patricia Dávila and Salvador Arias
Plants 2019, 8(10), 392; https://doi.org/10.3390/plants8100392 - 1 Oct 2019
Cited by 24 | Viewed by 3701
Abstract
The complete sequence of chloroplast genome (cpDNA) has been documented for single large columnar species of Cactaceae, lacking inverted repeats (IRs). We sequenced cpDNA for seven species of the short-globose cacti of Mammillaria and de novo assembly revealed three novel structures in land [...] Read more.
The complete sequence of chloroplast genome (cpDNA) has been documented for single large columnar species of Cactaceae, lacking inverted repeats (IRs). We sequenced cpDNA for seven species of the short-globose cacti of Mammillaria and de novo assembly revealed three novel structures in land plants. These structures have a large single copy (LSC) that is 2.5 to 10 times larger than the small single copy (SSC), and two IRs that contain strong differences in length and gene composition. Structure 1 is distinguished by short IRs of <1 kb composed by rpl23-trnI-CAU-ycf2; with a total length of 110,189 bp and 113 genes. In structure 2, each IR is approximately 7.2 kb and is composed of 11 genes and one Intergenic Spacer-(psbK-trnQ)-trnQ-UUG-rps16-trnK-UUU-matK-trnK-UUU-psbA-trnH-GUG-rpl2-rpl23-trnI-CAU-ycf2; with a total size of 116,175 bp and 120 genes. Structure 3 has divergent IRs of approximately 14.1 kb, where IRA is composed of 20 genes: psbA-trnH-GUG-rpl23-trnI-CAU-ycf2-ndhB-rps7-rps12-trnV-GAC-rrn16-ycf68-trnI-GAU-trnA-AGC-rrn23-rrn4.5-rrn5-trnR-ACG-trnN-GUU-ndhF-rpl32; and IRB is identical to the IRA, but lacks rpl23. This structure has 131 genes and, by pseudogenization, it is shown to have the shortest cpDNA, of just 107,343 bp. Our findings show that Mammillaria bears an unusual structural diversity of cpDNA, which supports the elucidation of the evolutionary processes involved in cacti lineages. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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Review

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10 pages, 468 KiB  
Review
Factors Affecting Organelle Genome Stability in Physcomitrella patens
by Masaki Odahara
Plants 2020, 9(2), 145; https://doi.org/10.3390/plants9020145 - 23 Jan 2020
Cited by 7 | Viewed by 2222
Abstract
Organelle genomes are essential for plants; however, the mechanisms underlying the maintenance of organelle genomes are incompletely understood. Using the basal land plant Physcomitrella patens as a model, nuclear-encoded homologs of bacterial-type homologous recombination repair (HRR) factors have been shown to play an [...] Read more.
Organelle genomes are essential for plants; however, the mechanisms underlying the maintenance of organelle genomes are incompletely understood. Using the basal land plant Physcomitrella patens as a model, nuclear-encoded homologs of bacterial-type homologous recombination repair (HRR) factors have been shown to play an important role in the maintenance of organelle genome stability by suppressing recombination between short dispersed repeats. In this review, I summarize the factors and pathways involved in the maintenance of genome stability, as well as the repeats that cause genomic instability in organelles in P. patens, and compare them with findings in other plant species. I also discuss the relationship between HRR factors and organelle genome structure from the evolutionary standpoint. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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28 pages, 6836 KiB  
Review
Structure–Function Analysis Reveals the Singularity of Plant Mitochondrial DNA Replication Components: A Mosaic and Redundant System
by Luis Gabriel Brieba
Plants 2019, 8(12), 533; https://doi.org/10.3390/plants8120533 - 21 Nov 2019
Cited by 10 | Viewed by 4419
Abstract
Plants are sessile organisms, and their DNA is particularly exposed to damaging agents. The integrity of plant mitochondrial and plastid genomes is necessary for cell survival. During evolution, plants have evolved mechanisms to replicate their mitochondrial genomes while minimizing the effects of DNA [...] Read more.
Plants are sessile organisms, and their DNA is particularly exposed to damaging agents. The integrity of plant mitochondrial and plastid genomes is necessary for cell survival. During evolution, plants have evolved mechanisms to replicate their mitochondrial genomes while minimizing the effects of DNA damaging agents. The recombinogenic character of plant mitochondrial DNA, absence of defined origins of replication, and its linear structure suggest that mitochondrial DNA replication is achieved by a recombination-dependent replication mechanism. Here, I review the mitochondrial proteins possibly involved in mitochondrial DNA replication from a structural point of view. A revision of these proteins supports the idea that mitochondrial DNA replication could be replicated by several processes. The analysis indicates that DNA replication in plant mitochondria could be achieved by a recombination-dependent replication mechanism, but also by a replisome in which primers are synthesized by three different enzymes: Mitochondrial RNA polymerase, Primase-Helicase, and Primase-Polymerase. The recombination-dependent replication model and primers synthesized by the Primase-Polymerase may be responsible for the presence of genomic rearrangements in plant mitochondria. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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18 pages, 1768 KiB  
Review
Plant Organelle Genome Replication
by Stewart A. Morley, Niaz Ahmad and Brent L. Nielsen
Plants 2019, 8(10), 358; https://doi.org/10.3390/plants8100358 - 21 Sep 2019
Cited by 37 | Viewed by 7397
Abstract
Mitochondria and chloroplasts perform essential functions in respiration, ATP production, and photosynthesis, and both organelles contain genomes that encode only some of the proteins that are required for these functions. The proteins and mechanisms for organelle DNA replication are very similar to bacterial [...] Read more.
Mitochondria and chloroplasts perform essential functions in respiration, ATP production, and photosynthesis, and both organelles contain genomes that encode only some of the proteins that are required for these functions. The proteins and mechanisms for organelle DNA replication are very similar to bacterial or phage systems. The minimal replisome may consist of DNA polymerase, a primase/helicase, and a single-stranded DNA binding protein (SSB), similar to that found in bacteriophage T7. In Arabidopsis, there are two genes for organellar DNA polymerases and multiple potential genes for SSB, but there is only one known primase/helicase protein to date. Genome copy number varies widely between type and age of plant tissues. Replication mechanisms are only poorly understood at present, and may involve multiple processes, including recombination-dependent replication (RDR) in plant mitochondria and perhaps also in chloroplasts. There are still important questions remaining as to how the genomes are maintained in new organelles, and how genome copy number is determined. This review summarizes our current understanding of these processes. Full article
(This article belongs to the Special Issue Plant Organelle DNA Maintenance)
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