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DNA Damage and Repair in Plants

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 July 2019) | Viewed by 49879

Special Issue Editors

Institut de Biologie Moleculaire des Plantes, Strasbourg, France
Interests: DNA repair; small RNA; genome-epigenome dynamics; abiotic stress
Special Issues, Collections and Topics in MDPI journals
Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
Interests: DNA repair; genome-epigenome dynamics; somatic homologous recombination; T.-DNA integration; environmental stress
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Due to their lifestyles, land and water plants have evolved sophisticated mechanisms to cope with environmental stresses that affect chromosome integrity. Hence, characterizing the dynamic responses of such living organisms to genotoxic stress will be of special importance for our understanding of their interactions with environmental cues.

The DNA repair machinery has to act in the context of chromatin; thus, the local chromatin landscape as well as its higher order structure can affect the DNA damage response. Therefore, it is crucial to understand how DNA repair pathways are regulated and coordinated by genetic and epigenetic factors in order to protect chromosomes against deleterious damage. This understanding is of critical value for basic as well as applied research.

This Special Issue calls for original articles, reviews, and perspectives that will allow unveiling how DNA repair pathways act in the context of chromatin to control genome stability/flexibility.

Dr. Jean Molinier
Prof. Dr. Barbara Hohn
Guest Editors

Manuscript Submission Information

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Keywords

  • Photosynthetic organisms
  • DNA damage
  • DNA repair
  • Chromatin
  • Genome
  • Epigenome
  • Genome editing

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Published Papers (10 papers)

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Research

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10 pages, 2628 KiB  
Article
Single Molecule Imaging of T-DNA Intermediates Following Agrobacterium tumefaciens Infection in Nicotiana benthamiana
by Idan Pereman, Cathy Melamed-Bessudo, Tal Dahan-Meir, Elad Herz, Michael Elbaum and Avraham A. Levy
Int. J. Mol. Sci. 2019, 20(24), 6209; https://doi.org/10.3390/ijms20246209 - 09 Dec 2019
Cited by 3 | Viewed by 3473
Abstract
Plant transformation mediated by Agrobacterium tumefaciens is a well-studied phenomenon in which a bacterial DNA fragment (T-DNA), is transferred to the host plant cell, as a single strand, via type IV secretion system and has the potential to reach the nucleus and to [...] Read more.
Plant transformation mediated by Agrobacterium tumefaciens is a well-studied phenomenon in which a bacterial DNA fragment (T-DNA), is transferred to the host plant cell, as a single strand, via type IV secretion system and has the potential to reach the nucleus and to be integrated into its genome. While Agrobacterium-mediated transformation has been widely used for laboratory-research and in breeding, the time-course of its journey from the bacterium to the nucleus, the conversion from single- to double-strand intermediates and several aspects of the integration in the genome remain obscure. In this study, we sought to follow T-DNA infection directly using single-molecule live imaging. To this end, we applied the LacO-LacI imaging system in Nicotiana benthamiana, which enabled us to identify double-stranded T-DNA (dsT-DNA) molecules as fluorescent foci. Using confocal microscopy, we detected progressive accumulation of dsT-DNA foci in the nucleus, starting 23 h after transfection and reaching an average of 5.4 and 8 foci per nucleus at 48 and 72 h post-infection, respectively. A time-course diffusion analysis of the T-DNA foci has demonstrated their spatial confinement. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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17 pages, 7008 KiB  
Article
ZmRAD51C Is Essential for Double-Strand Break Repair and Homologous Recombination in Maize Meiosis
by Juli Jing, Ting Zhang, Yazhong Wang, Zhenhai Cui and Yan He
Int. J. Mol. Sci. 2019, 20(21), 5513; https://doi.org/10.3390/ijms20215513 - 05 Nov 2019
Cited by 15 | Viewed by 4085
Abstract
Radiation sensitive 51 (RAD51) recombinases play crucial roles in meiotic double-strand break (DSB) repair mediated by homologous recombination (HR) to ensure the correct segregation of homologous chromosomes. In this study, we identified the meiotic functions of ZmRAD51C, the maize homolog of Arabidopsis [...] Read more.
Radiation sensitive 51 (RAD51) recombinases play crucial roles in meiotic double-strand break (DSB) repair mediated by homologous recombination (HR) to ensure the correct segregation of homologous chromosomes. In this study, we identified the meiotic functions of ZmRAD51C, the maize homolog of Arabidopsis and rice RAD51C. The Zmrad51c mutants exhibited regular vegetative growth but complete sterility for both male and female inflorescence. However, the mutants showed hypersensitivity to DNA damage by mitomycin C. Cytological analysis indicated that homologous chromosome pairing and synapsis were rigorously inhibited, and meiotic chromosomes were often entangled from diplotene to metaphase I, leading to chromosome fragmentation at anaphase I. Immunofluorescence analysis showed that although the signals of the axial element absence of first division (AFD1) and asynaptic1 (ASY1) were normal, the assembly of the central element zipper1 (ZYP1) was severely disrupted. The DSB formation was normal in Zmrad51c meiocytes, symbolized by the regular occurrence of γH2AX signals. However, RAD51 and disrupted meiotic cDNA 1 (DMC1) signals were never detected at the early stage of prophase I in the mutant. Taken together, our results indicate that ZmRAD51C functions crucially for both meiotic DSB repair and homologous recombination in maize. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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26 pages, 4545 KiB  
Article
Global Transcriptome and Co-Expression Network Analysis Reveal Contrasting Response of Japonica and Indica Rice Cultivar to γ Radiation
by Xiaoxiang Zhang, Niansheng Huang, Lanjing Mo, Minjia Lv, Yingbo Gao, Junpeng Wang, Chang Liu, Shuangyi Yin, Juan Zhou, Ning Xiao, Cunhong Pan, Yabin Xu, Guichun Dong, Zefeng Yang, Aihong Li, Jianye Huang, Yulong Wang and Youli Yao
Int. J. Mol. Sci. 2019, 20(18), 4358; https://doi.org/10.3390/ijms20184358 - 05 Sep 2019
Cited by 7 | Viewed by 3181
Abstract
Japonica and indica are two important subspecies in cultivated Asian rice. Irradiation is a classical approach to induce mutations and create novel germplasm. However, little is known about the differential response between japonica and indica rice after γ radiation. Here, we utilized the [...] Read more.
Japonica and indica are two important subspecies in cultivated Asian rice. Irradiation is a classical approach to induce mutations and create novel germplasm. However, little is known about the differential response between japonica and indica rice after γ radiation. Here, we utilized the RNA sequencing and Weighted Gene Co-expression Network Analysis (WGCNA) to compare the transcriptome differences between japonica Nipponbare (NPB) and indica Yangdao6 (YD6) in response to irradiation. Japonica subspecies are more sensitive to irradiation than the indica subspecies. Indica showed a higher seedling survival rate than japonica. Irradiation caused more extensive DNA damage in shoots than in roots, and the severity was higher in NPB than in YD6. GO and KEGG pathway analyses indicate that the core genes related to DNA repair and replication and cell proliferation are similarly regulated between the varieties, however the universal stress responsive genes show contrasting differential response patterns in japonica and indica. WGCNA identifies 37 co-expressing gene modules and ten candidate hub genes for each module. This provides novel evidence indicating that certain peripheral pathways may dominate the molecular networks in irradiation survival and suggests more potential target genes in breeding for universal stress tolerance in rice. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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13 pages, 1104 KiB  
Article
Detecting Brachypodium distachyon Chromosomes Bd4 and Bd5 in MH- and X-Ray-Induced Micronuclei Using mcFISH
by Arita Kus, Joanna Szymanowska-Pułka, Jolanta Kwasniewska and Robert Hasterok
Int. J. Mol. Sci. 2019, 20(11), 2848; https://doi.org/10.3390/ijms20112848 - 11 Jun 2019
Cited by 6 | Viewed by 3441
Abstract
Micronuclei are biomarkers of genotoxic effects and chromosomal instability. They are formed when chromosome fragments or whole chromosomes fail to disjoin into daughter nuclei. We present qualitative and quantitative analyses of the involvement of specific chromosome regions of chromosomes Bd4 and Bd5 in [...] Read more.
Micronuclei are biomarkers of genotoxic effects and chromosomal instability. They are formed when chromosome fragments or whole chromosomes fail to disjoin into daughter nuclei. We present qualitative and quantitative analyses of the involvement of specific chromosome regions of chromosomes Bd4 and Bd5 in the formation of micronuclei of Brachypodium distachyon root tip cells following maleic hydrazide (MH) treatment and X-radiation. This is visualised by cytomolecular approaches using bacterial artificial chromosome (BAC)-based multicolour fluorescence in situ hybridisation (mcFISH) in combination with 5S and 25S rDNA probes. The results showed that the long arm of submetacentric chromosome Bd4 forms micronuclei at twice the frequency of its short arm, suggesting that the former is more prone to double-strand breaks (DSBs). In contrast, no difference was observed in the frequency of micronuclei derived from the long and short arms of submetacentric chromosome Bd5. Interestingly, the proximal region of the short arm of Bd5 is more prone to DSBs than its distal part. This demonstrates that 5S rDNA and 35S rDNA loci are not “hot spots” for DNA breaks after the application of these mutagens. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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Review

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24 pages, 1000 KiB  
Review
DNA Repair and the Stability of the Plant Mitochondrial Genome
by Nicolas Chevigny, Déborah Schatz-Daas, Frédérique Lotfi and José Manuel Gualberto
Int. J. Mol. Sci. 2020, 21(1), 328; https://doi.org/10.3390/ijms21010328 - 03 Jan 2020
Cited by 76 | Viewed by 6815
Abstract
The mitochondrion stands at the center of cell energy metabolism. It contains its own genome, the mtDNA, that is a relic of its prokaryotic symbiotic ancestor. In plants, the mitochondrial genetic information influences important agronomic traits including fertility, plant vigor, chloroplast function, and [...] Read more.
The mitochondrion stands at the center of cell energy metabolism. It contains its own genome, the mtDNA, that is a relic of its prokaryotic symbiotic ancestor. In plants, the mitochondrial genetic information influences important agronomic traits including fertility, plant vigor, chloroplast function, and cross-compatibility. Plant mtDNA has remarkable characteristics: It is much larger than the mtDNA of other eukaryotes and evolves very rapidly in structure. This is because of recombination activities that generate alternative mtDNA configurations, an important reservoir of genetic diversity that promotes rapid mtDNA evolution. On the other hand, the high incidence of ectopic recombination leads to mtDNA instability and the expression of gene chimeras, with potential deleterious effects. In contrast to the structural plasticity of the genome, in most plant species the mtDNA coding sequences evolve very slowly, even if the organization of the genome is highly variable. Repair mechanisms are probably responsible for such low mutation rates, in particular repair by homologous recombination. Herein we review some of the characteristics of plant organellar genomes and of the repair pathways found in plant mitochondria. We further discuss how homologous recombination is involved in the evolution of the plant mtDNA. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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25 pages, 3796 KiB  
Review
Plant DNA Polymerases
by Jose-Antonio Pedroza-Garcia, Lieven De Veylder and Cécile Raynaud
Int. J. Mol. Sci. 2019, 20(19), 4814; https://doi.org/10.3390/ijms20194814 - 27 Sep 2019
Cited by 14 | Viewed by 5164
Abstract
Maintenance of genome integrity is a key process in all organisms. DNA polymerases (Pols) are central players in this process as they are in charge of the faithful reproduction of the genetic information, as well as of DNA repair. Interestingly, all eukaryotes possess [...] Read more.
Maintenance of genome integrity is a key process in all organisms. DNA polymerases (Pols) are central players in this process as they are in charge of the faithful reproduction of the genetic information, as well as of DNA repair. Interestingly, all eukaryotes possess a large repertoire of polymerases. Three protein complexes, DNA Pol α, δ, and ε, are in charge of nuclear DNA replication. These enzymes have the fidelity and processivity required to replicate long DNA sequences, but DNA lesions can block their progression. Consequently, eukaryotic genomes also encode a variable number of specialized polymerases (between five and 16 depending on the organism) that are involved in the replication of damaged DNA, DNA repair, and organellar DNA replication. This diversity of enzymes likely stems from their ability to bypass specific types of lesions. In the past 10–15 years, our knowledge regarding plant DNA polymerases dramatically increased. In this review, we discuss these recent findings and compare acquired knowledge in plants to data obtained in other eukaryotes. We also discuss the emerging links between genome and epigenome replication. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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17 pages, 1269 KiB  
Review
Advances Towards How Meiotic Recombination Is Initiated: A Comparative View and Perspectives for Plant Meiosis Research
by Ju-Li Jing, Ting Zhang, Ya-Zhong Wang and Yan He
Int. J. Mol. Sci. 2019, 20(19), 4718; https://doi.org/10.3390/ijms20194718 - 23 Sep 2019
Cited by 6 | Viewed by 5290
Abstract
Meiosis is an essential cell-division process for ensuring genetic diversity across generations. Meiotic recombination ensures the accuracy of genetic interchange between homolous chromosomes and segregation of parental alleles. Programmed DNA double-strand breaks (DSBs), catalyzed by the evolutionarily conserved topoisomerase VIA (a subunit of [...] Read more.
Meiosis is an essential cell-division process for ensuring genetic diversity across generations. Meiotic recombination ensures the accuracy of genetic interchange between homolous chromosomes and segregation of parental alleles. Programmed DNA double-strand breaks (DSBs), catalyzed by the evolutionarily conserved topoisomerase VIA (a subunit of the archaeal type II DNA topoisomerase)-like enzyme Spo11 and several other factors, is a distinctive feature of meiotic recombination initiation. The meiotic DSB formation and its regulatory mechanisms are similar among species, but certain aspects are distinct. In this review, we introduced the cumulative knowledge of the plant proteins crucial for meiotic DSB formation and technical advances in DSB detection. We also summarized the genome-wide DSB hotspot profiles for different model organisms. Moreover, we highlighted the classical views and recent advances in our knowledge of the regulatory mechanisms that ensure the fidelity of DSB formation, such as multifaceted kinase-mediated phosphorylation and the consequent high-dimensional changes in chromosome structure. We provided an overview of recent findings concerning DSB formation, distribution and regulation, all of which will help us to determine whether meiotic DSB formation is evolutionarily conserved or varies between plants and other organisms. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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19 pages, 1295 KiB  
Review
Active DNA Demethylation in Plants
by Jara Teresa Parrilla-Doblas, Teresa Roldán-Arjona, Rafael R. Ariza and Dolores Córdoba-Cañero
Int. J. Mol. Sci. 2019, 20(19), 4683; https://doi.org/10.3390/ijms20194683 - 21 Sep 2019
Cited by 36 | Viewed by 4370
Abstract
Methylation of cytosine (5-meC) is a critical epigenetic modification in many eukaryotes, and genomic DNA methylation landscapes are dynamically regulated by opposed methylation and demethylation processes. Plants are unique in possessing a mechanism for active DNA demethylation involving DNA glycosylases that excise 5-meC [...] Read more.
Methylation of cytosine (5-meC) is a critical epigenetic modification in many eukaryotes, and genomic DNA methylation landscapes are dynamically regulated by opposed methylation and demethylation processes. Plants are unique in possessing a mechanism for active DNA demethylation involving DNA glycosylases that excise 5-meC and initiate its replacement with unmodified C through a base excision repair (BER) pathway. Plant BER-mediated DNA demethylation is a complex process involving numerous proteins, as well as additional regulatory factors that avoid accumulation of potentially harmful intermediates and coordinate demethylation and methylation to maintain balanced yet flexible DNA methylation patterns. Active DNA demethylation counteracts excessive methylation at transposable elements (TEs), mainly in euchromatic regions, and one of its major functions is to avoid methylation spreading to nearby genes. It is also involved in transcriptional activation of TEs and TE-derived sequences in companion cells of male and female gametophytes, which reinforces transposon silencing in gametes and also contributes to gene imprinting in the endosperm. Plant 5-meC DNA glycosylases are additionally involved in many other physiological processes, including seed development and germination, fruit ripening, and plant responses to a variety of biotic and abiotic environmental stimuli. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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19 pages, 1807 KiB  
Review
DNA- and DNA-Protein-Crosslink Repair in Plants
by Janina Enderle, Annika Dorn and Holger Puchta
Int. J. Mol. Sci. 2019, 20(17), 4304; https://doi.org/10.3390/ijms20174304 - 03 Sep 2019
Cited by 14 | Viewed by 6515
Abstract
DNA-crosslinks are one of the most severe types of DNA lesions. Crosslinks (CLs) can be subdivided into DNA-intrastrand CLs, DNA-interstrand CLs (ICLs) and DNA-protein crosslinks (DPCs), and arise by various exogenous and endogenous sources. If left unrepaired before the cell enters S-phase, ICLs [...] Read more.
DNA-crosslinks are one of the most severe types of DNA lesions. Crosslinks (CLs) can be subdivided into DNA-intrastrand CLs, DNA-interstrand CLs (ICLs) and DNA-protein crosslinks (DPCs), and arise by various exogenous and endogenous sources. If left unrepaired before the cell enters S-phase, ICLs and DPCs pose a major threat to genomic integrity by blocking replication. In order to prevent the collapse of replication forks and impairment of cell division, complex repair pathways have emerged. In mammals, ICLs are repaired by the so-called Fanconi anemia (FA) pathway, which includes 22 different FANC genes, while in plants only a few of these genes are conserved. In this context, two pathways of ICL repair have been defined, each requiring the interaction of a helicase (FANCJB/RTEL1) and a nuclease (FAN1/MUS81). Moreover, homologous recombination (HR) as well as postreplicative repair factors are also involved. Although DPCs possess a comparable toxic potential to cells, it has only recently been shown that at least three parallel pathways for DPC repair exist in plants, defined by the protease WSS1A, the endonuclease MUS81 and tyrosyl-DNA phosphodiesterase 1 (TDP1). The importance of crosslink repair processes are highlighted by the fact that deficiencies in the respective pathways are associated with diverse hereditary disorders. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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22 pages, 1085 KiB  
Review
Chromatin Remodeling and Epigenetic Regulation in Plant DNA Damage Repair
by Jin-Hong Kim
Int. J. Mol. Sci. 2019, 20(17), 4093; https://doi.org/10.3390/ijms20174093 - 22 Aug 2019
Cited by 43 | Viewed by 6486
Abstract
DNA damage response (DDR) in eukaryotic cells is initiated in the chromatin context. DNA damage and repair depend on or have influence on the chromatin dynamics associated with genome stability. Epigenetic modifiers, such as chromatin remodelers, histone modifiers, DNA (de-)methylation enzymes, and noncoding [...] Read more.
DNA damage response (DDR) in eukaryotic cells is initiated in the chromatin context. DNA damage and repair depend on or have influence on the chromatin dynamics associated with genome stability. Epigenetic modifiers, such as chromatin remodelers, histone modifiers, DNA (de-)methylation enzymes, and noncoding RNAs regulate DDR signaling and DNA repair by affecting chromatin dynamics. In recent years, significant progress has been made in the understanding of plant DDR and DNA repair. SUPPRESSOR OF GAMMA RESPONSE1, RETINOBLASTOMA RELATED1 (RBR1)/E2FA, and NAC103 have been proven to be key players in the mediation of DDR signaling in plants, while plant-specific chromatin remodelers, such as DECREASED DNA METHYLATION1, contribute to chromatin dynamics for DNA repair. There is accumulating evidence that plant epigenetic modifiers are involved in DDR and DNA repair. In this review, I examine how DDR and DNA repair machineries are concertedly regulated in Arabidopsis thaliana by a variety of epigenetic modifiers directing chromatin remodeling and epigenetic modification. This review will aid in updating our knowledge on DDR and DNA repair in plants. Full article
(This article belongs to the Special Issue DNA Damage and Repair in Plants)
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