DNA Damage Responses in Plants

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (31 October 2017) | Viewed by 45655

Special Issue Editors


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Guest Editor
Department of Biology and Biotechnology ‘Lazzaro Spallanzani’, University of Pavia, via Ferrata 9, 27100 Pavia, Italy
Interests: seed germination; DNA repair; genotoxic stress; antioxidant response
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Guest Editor
Instituto de Tecnologia Química e Biológica António Xavier (ITQB-NOVA), Oeiras, Portugal
Interests: abiotic stress responses in plants; seed development; seed invigoration; systems biology; genome integrity; regulation of gene expression
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Gregor Mendel Institute (GMI) Austrian Academy of Science, Vienna Biocenter (VBC), Dr. Bohr Gasse 3, 1030 Vienna, Austria
Interests: chromatin remodeling; epigenetic modifications; meiotic and somatic recombination; diRNAs; endoreduplication; transposable elements; cell cycle

Special Issue Information

Dear Colleagues,

Maintenance of genome integrity represents a priority for all living organisms that are exposed to genotoxic stress triggered by metabolic by-products and DNA replication stress, as well as environmental chemical pollutants (pesticides, herbicides, heavy metals, ozone) and physical agents (UV and ionizing radiation). Genomic instability results from the accumulation of lesions that cause structural damage to DNA, impairing fundamental cellular processes, such as DNA replication and transcription. DNA damage includes base and sugar modifications, single- and double-strand breaks, DNA-protein cross-links, and abasic sites. Similar to the other eukaryotes, plants have evolved highly conserved, specialized DNA repair pathways (base excision repair, mismatch repair, nucleotide excision repair, and double-strand break repair which comprises both homologous recombination and non-homologous end-joining), targeting the different types of lesions to ensure the integrity of genetic information. However, being sessile organisms, plants are continuously exposed to genotoxic stress and their peculiar photosynthetic activity, localized within chloroplasts, is a constant source of reactive oxygen species and is extremely harmful to lipids, proteins and nucleic acids.

DNA damage response (DDR) is the sum of multiple cellular pathways, triggered on DNA damage detection in order to activate downstream mechanisms allowing the temporary cell cycle arrest and DNA repair. When damage is accumulated above a critical threshold and DNA repair is not able to reverse lesions, cells undergo programmed cell death, avoiding genetic defects that might impair plant development or limit crop performance in terms of seed quality and yields. In this context, DDR systems act as crucial regulators of cell cycle checkpoints, revealing that DNA damage sensing and signaling are strictly linked to growth. DNA lesions contribute to cell aging and there is renewed interest in plant telomere biology in the context of DNA repair and recombination. Plants can also better withstand genotoxic injury by activating endoreduplication mechanisms. Plant genomes host highly conserved DDR components, both regulators and effectors, but there are several plant-specific features of DDR that make this process unique compared to animals.

This Special Issue aims at providing an update of the last findings in basic and applied plant DDR research on model and crop plants investigated in vitro and/or in the field, under abiotic and biotic stress conditions or exposed to specific genotoxins. Original research articles, research notes, and review articles are welcomed.

Manuscripts should address, but are not restricted to the following topics:

  • Relevance of microRNAs in DNA damage response
  • Molecular mechanisms underlying DNA damage sensing and repair in plants
  • The DNA damage response in seeds
  • DNA repair in the context of genome editing
  • Genotoxic effects of abiotic stress
  • High-throughput approaches for the study of the DNA damage response in plants
  • The epigenetic components of the DNA damage response
  • Plant telomeres
  • The plant nucleolus
  • The DNA damage response in the context of mutation breeding
  • Bioinformatics tools for the study of DNA repair
  • Models for investigating DNA repair and mutagenesis mechanisms in plants
  • Transcription hubs controlling the DNA damage response

Dr. Alma Balestrazzi
Dr. Susana Araújo
Dr. Mattia Donà
Guest Editors

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Published Papers (9 papers)

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Research

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24 pages, 4536 KiB  
Article
Maintaining Genome Integrity during Seed Development in Phaseolus vulgaris L.: Evidence from a Transcriptomic Profiling Study
by José Ricardo Parreira, Alma Balestrazzi, Pedro Fevereiro and Susana De Sousa Araújo
Genes 2018, 9(10), 463; https://doi.org/10.3390/genes9100463 - 20 Sep 2018
Cited by 14 | Viewed by 3642
Abstract
The maintenance of genome integrity is crucial in seeds, due to the constant challenge of several endogenous and exogenous factors. The knowledge concerning DNA damage response and chromatin remodeling during seed development is still scarce, especially in Phaseolus vulgaris L. A transcriptomic profiling [...] Read more.
The maintenance of genome integrity is crucial in seeds, due to the constant challenge of several endogenous and exogenous factors. The knowledge concerning DNA damage response and chromatin remodeling during seed development is still scarce, especially in Phaseolus vulgaris L. A transcriptomic profiling of the expression of genes related to DNA damage response/chromatin remodeling mechanisms was performed in P. vulgaris seeds at four distinct developmental stages, spanning from late embryogenesis to seed desiccation. Of the 14,001 expressed genes identified using massive analysis of cDNA ends, 301 belong to the DNA MapMan category. In late embryogenesis, a high expression of genes related to DNA damage sensing and repair suggests there is a tight control of DNA integrity. At the end of filling and the onset of seed dehydration, the upregulation of genes implicated in sensing of DNA double-strand breaks suggests that genome integrity is challenged. The expression of chromatin remodelers seems to imply a concomitant action of chromatin remodeling with DNA repair machinery, maintaining genome stability. The expression of genes related to nucleotide excision repair and chromatin structure is evidenced during the desiccation stage. An overview of the genes involved in DNA damage response and chromatin remodeling during P. vulgaris seed development is presented, providing insights into the mechanisms used by developing seeds to cope with DNA damage. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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13 pages, 1284 KiB  
Article
In silico Phylogenetic Analysis of hAT Transposable Elements in Plants
by Gökhan Karakülah and Athanasia Pavlopoulou
Genes 2018, 9(6), 284; https://doi.org/10.3390/genes9060284 - 6 Jun 2018
Cited by 8 | Viewed by 5200
Abstract
Transposable elements of the hAT family exhibit a cross-kingdom distribution. The plant hAT transposons are proposed to play a critical role in plant adaptive evolution and DNA damage repair. The sequencing of an increasing number of plant genomes has facilitated the discovery of [...] Read more.
Transposable elements of the hAT family exhibit a cross-kingdom distribution. The plant hAT transposons are proposed to play a critical role in plant adaptive evolution and DNA damage repair. The sequencing of an increasing number of plant genomes has facilitated the discovery of a plethora of hAT elements. This enabled us to perform an in-depth phylogenetic analysis of consensus hAT sequences in the fully-sequenced genomes of 11 plant species that represent diverse taxonomic divisions. Four putative nucleotide sequences were detected in cottonwood that were similar to the corresponding animal hAT elements, which are possibly sequence artifacts. Phylogenetic trees were constructed based both on the known and putative hAT sequences, by employing two different methods of phylogenetic inference. On the basis of the reconstructed phylogeny, plant hAT elements have rather evolved through kingdom-specific vertical gene transfer and gene amplifications within eudicotyledons, monocotyledons, and chlorophytes. Furthermore, the plant hAT sequences were searched for conserved DNA and amino acid sequence features. In this way, diagnostic sequence patterns were detected which allowed us to assign functional annotations to the plant hAT sequences. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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18 pages, 2910 KiB  
Article
The Human Tyrosyl-DNA Phosphodiesterase 1 (hTdp1) Inhibitor NSC120686 as an Exploratory Tool to Investigate Plant Tdp1 Genes
by Anca Macovei, Andrea Pagano, Maria Elisa Sabatini, Sofia Grandi and Alma Balestrazzi
Genes 2018, 9(4), 186; https://doi.org/10.3390/genes9040186 - 28 Mar 2018
Cited by 7 | Viewed by 3815
Abstract
The hTdp1 (human tyrosyl-DNA phosphodiesterase 1) inhibitor NSC120686 has been used, along with topoisomerase inhibitors, as a pharmacophoric model to restrain the Tdp1 activity as part of a synergistic treatment for cancer. While this compound has an end-point application in medical research, in [...] Read more.
The hTdp1 (human tyrosyl-DNA phosphodiesterase 1) inhibitor NSC120686 has been used, along with topoisomerase inhibitors, as a pharmacophoric model to restrain the Tdp1 activity as part of a synergistic treatment for cancer. While this compound has an end-point application in medical research, in plants, its application has not been considered so far. The originality of our study consists in the use of hTdp1 inhibitor in Medicago truncatula cells, which, unlike human cells, contain two Tdp1 genes. Hence, the purpose of this study was to test the hTdp1 inhibitor NSC120686 as an exploratory tool to investigate the plant Tdp1 genes, since their characterization is still in incipient phases. To do so, M. truncatula calli were exposed to increasing (75, 150, 300 μM) concentrations of NSC120686. The levels of cell mortality and DNA damage, measured via diffusion assay and comet assay, respectively, were significantly increased when the highest doses were used, indicative of a cytotoxic and genotoxic threshold. In addition, the NSC120686-treated calli and untreated MtTdp1α-depleted calli shared a similar response in terms of programmed cell death (PCD)/necrosis and DNA damage. Interestingly, the expression profiles of MtTdp1α and MtTdp1β genes were differently affected by the NSC120686 treatment, as MtTdp1α was upregulated while MtTdp1β was downregulated. The NSC120686 treatment affected not only the MtTdp1 genes but also other genes with roles in alternative DNA repair pathways. Since the expression patterns of these genes were different than what was observed in the MtTdp1α-depleted plants, it could be hypothesized that the NSC120686 treatment exerts a different influence compared to that resulting from the lack of the MtTdp1α gene function. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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11 pages, 1981 KiB  
Article
The Moss Physcomitrella patens Is Hyperresistant to DNA Double-Strand Breaks Induced by γ-Irradiation
by Yuichiro Yokota and Ayako N. Sakamoto
Genes 2018, 9(2), 76; https://doi.org/10.3390/genes9020076 - 7 Feb 2018
Cited by 6 | Viewed by 4098
Abstract
The purpose of this study was to investigate whether the moss Physcomitrella patens cells are more resistant to ionizing radiation than animal cells. Protoplasts derived from P. patens protonemata were irradiated with γ-rays of 50–1000 gray (Gy). Clonogenicity of the protoplasts decreased in [...] Read more.
The purpose of this study was to investigate whether the moss Physcomitrella patens cells are more resistant to ionizing radiation than animal cells. Protoplasts derived from P. patens protonemata were irradiated with γ-rays of 50–1000 gray (Gy). Clonogenicity of the protoplasts decreased in a γ-ray dose-dependent manner. The dose that decreased clonogenicity by half (LD50) was 277 Gy, which indicated that the moss protoplasts were 200-times more radioresistant than human cells. To investigate the mechanism of radioresistance in P. patens, we irradiated protoplasts on ice and initial double-strand break (DSB) yields were measured using the pulsed-field gel electrophoresis assay. Induced DSBs linearly increased dependent on the γ-ray dose and the DSB yield per Gb DNA per Gy was 2.2. The DSB yield in P. patens was half to one-third of those reported in mammals and yeasts, indicating that DSBs are difficult to induce in P. patens. The DSB yield per cell per LD50 dose in P. patens was 311, which is three- to six-times higher than those in mammals and yeasts, implying that P. patens is hyperresistant to DSBs. Physcomitrella patens is indicated to possess unique mechanisms to inhibit DSB induction and provide resistance to high numbers of DSBs. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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3250 KiB  
Article
RAD4 and RAD23/HMR Contribute to Arabidopsis UV Tolerance
by Triparna Lahari, Janelle Lazaro and Dana F. Schroeder
Genes 2018, 9(1), 8; https://doi.org/10.3390/genes9010008 - 28 Dec 2017
Cited by 15 | Viewed by 4960
Abstract
In plants, exposure to solar ultraviolet (UV) light is unavoidable, resulting in DNA damage. Damaged DNA causes mutations, replication arrest, and cell death, thus efficient repair of the damaged DNA is essential. A light-independent DNA repair pathway called nucleotide excision repair (NER) is [...] Read more.
In plants, exposure to solar ultraviolet (UV) light is unavoidable, resulting in DNA damage. Damaged DNA causes mutations, replication arrest, and cell death, thus efficient repair of the damaged DNA is essential. A light-independent DNA repair pathway called nucleotide excision repair (NER) is conserved throughout evolution. For example, the damaged DNA-binding protein Radiation sensitive 4 (Rad4) in Saccharomyces cerevisiae is homologous to the mammalian NER protein Xeroderma Pigmentosum complementation group C (XPC). In this study, we examined the role of the Arabidopsis thaliana Rad4/XPC homologue (AtRAD4) in plant UV tolerance by generating overexpression lines. AtRAD4 overexpression, both with and without an N-terminal yellow fluorescent protein (YFP) tag, resulted in increased UV tolerance. YFP-RAD4 localized to the nucleus, and UV treatment did not alter this localization. We also used yeast two-hybrid analysis to examine the interaction of AtRAD4 with Arabidopsis RAD23 and found that RAD4 interacted with RAD23B as well as with the structurally similar protein HEMERA (HMR). In addition, we found that hmr and rad23 mutants exhibited increased UV sensitivity. Thus, our analysis suggests a role for RAD4 and RAD23/HMR in plant UV tolerance. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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2539 KiB  
Article
Evolutionarily Distant Streptophyta Respond Differently to Genotoxic Stress
by Radka Vágnerová, Alena Lukešová, Martin Lukeš, Petra Rožnovská, Marcela Holá, Jana Fulnečková, Jiří Fajkus and Karel J. Angelis
Genes 2017, 8(11), 331; https://doi.org/10.3390/genes8110331 - 17 Nov 2017
Cited by 2 | Viewed by 5243
Abstract
Research in algae usually focuses on the description and characterization of morpho—and phenotype as a result of adaptation to a particular habitat and its conditions. To better understand the evolution of lineages we characterized responses of filamentous streptophyte green algae of the genera [...] Read more.
Research in algae usually focuses on the description and characterization of morpho—and phenotype as a result of adaptation to a particular habitat and its conditions. To better understand the evolution of lineages we characterized responses of filamentous streptophyte green algae of the genera Klebsormidium and Zygnema, and of a land plant—the moss Physcomitrella patens—to genotoxic stress that might be relevant to their environment. We studied the induction and repair of DNA double strand breaks (DSBs) elicited by the radiomimetic drug bleomycin, DNA single strand breaks (SSB) as consequence of base modification by the alkylation agent methyl methanesulfonate (MMS) and of ultra violet (UV)-induced photo-dimers, because the mode of action of these three genotoxic agents is well understood. We show that the Klebsormidium and Physcomitrella are similarly sensitive to introduced DNA lesions and have similar rates of DSBs repair. In contrast, less DNA damage and higher repair rate of DSBs was detected in Zygnema, suggesting different mechanisms of maintaining genome integrity in response to genotoxic stress. Nevertheless, contrary to fewer detected lesions is Zygnema more sensitive to genotoxic treatment than Klebsormidium and Physcomitrella Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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Review

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16 pages, 2028 KiB  
Review
Scaffolding for Repair: Understanding Molecular Functions of the SMC5/6 Complex
by Mariana Diaz and Ales Pecinka
Genes 2018, 9(1), 36; https://doi.org/10.3390/genes9010036 - 12 Jan 2018
Cited by 33 | Viewed by 7413
Abstract
Chromosome organization, dynamics and stability are required for successful passage through cellular generations and transmission of genetic information to offspring. The key components involved are Structural maintenance of chromosomes (SMC) complexes. Cohesin complex ensures proper chromatid alignment, condensin complex chromosome condensation and the [...] Read more.
Chromosome organization, dynamics and stability are required for successful passage through cellular generations and transmission of genetic information to offspring. The key components involved are Structural maintenance of chromosomes (SMC) complexes. Cohesin complex ensures proper chromatid alignment, condensin complex chromosome condensation and the SMC5/6 complex is specialized in the maintenance of genome stability. Here we summarize recent knowledge on the composition and molecular functions of SMC5/6 complex. SMC5/6 complex was originally identified based on the sensitivity of its mutants to genotoxic stress but there is increasing number of studies demonstrating its roles in the control of DNA replication, sister chromatid resolution and genomic location-dependent promotion or suppression of homologous recombination. Some of these functions appear to be due to a very dynamic interaction with cohesin or other repair complexes. Studies in Arabidopsis indicate that, besides its canonical function in repair of damaged DNA, the SMC5/6 complex plays important roles in regulating plant development, abiotic stress responses, suppression of autoimmune responses and sexual reproduction. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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3339 KiB  
Review
Genome and Epigenome Surveillance Processes Underlying UV Exposure in Plants
by Jean Molinier
Genes 2017, 8(11), 316; https://doi.org/10.3390/genes8110316 - 9 Nov 2017
Cited by 19 | Viewed by 4540
Abstract
Land plants and other photosynthetic organisms (algae, bacteria) use the beneficial effect of sunlight as a source of energy for the photosynthesis and as a major source of information from the environment. However, the ultraviolet component of sunlight also produces several types of [...] Read more.
Land plants and other photosynthetic organisms (algae, bacteria) use the beneficial effect of sunlight as a source of energy for the photosynthesis and as a major source of information from the environment. However, the ultraviolet component of sunlight also produces several types of damage, which can affect cellular and integrity, interfering with growth and development. In order to reduce the deleterious effects of UV, photosynthetic organisms combine physiological adaptation and several types of DNA repair pathways to avoid dramatic changes in the structure. Therefore, plants may have obtained an evolutionary benefit from combining genome and surveillance processes, to efficiently deal with the deleterious effects of UV radiation. This review will present the different mechanisms activated upon UV exposure that contribute to maintain genome and integrity. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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3277 KiB  
Review
DNA Damage Repair System in Plants: A Worldwide Research Update
by Estela Gimenez and Francisco Manzano-Agugliaro
Genes 2017, 8(11), 299; https://doi.org/10.3390/genes8110299 - 30 Oct 2017
Cited by 35 | Viewed by 5253
Abstract
Living organisms are usually exposed to various DNA damaging agents so the mechanisms to detect and repair diverse DNA lesions have developed in all organisms with the result of maintaining genome integrity. Defects in DNA repair machinery contribute to cancer, certain diseases, and [...] Read more.
Living organisms are usually exposed to various DNA damaging agents so the mechanisms to detect and repair diverse DNA lesions have developed in all organisms with the result of maintaining genome integrity. Defects in DNA repair machinery contribute to cancer, certain diseases, and aging. Therefore, conserving the genomic sequence in organisms is key for the perpetuation of life. The machinery of DNA damage repair (DDR) in prokaryotes and eukaryotes is similar. Plants also share mechanisms for DNA repair with animals, although they differ in other important details. Plants have, surprisingly, been less investigated than other living organisms in this context, despite the fact that numerous lethal mutations in animals are viable in plants. In this manuscript, a worldwide bibliometric analysis of DDR systems and DDR research in plants was made. A comparison between both subjects was accomplished. The bibliometric analyses prove that the first study about DDR systems in plants (1987) was published thirteen years later than that for other living organisms (1975). Despite the increase in the number of papers about DDR mechanisms in plants in recent decades, nowadays the number of articles published each year about DDR systems in plants only represents 10% of the total number of articles about DDR. The DDR research field was done by 74 countries while the number of countries involved in the DDR & Plant field is 44. This indicates the great influence that DDR research in the plant field currently has, worldwide. As expected, the percentage of studies published about DDR systems in plants has increased in the subject area of agricultural and biological sciences and has diminished in medicine with respect to DDR studies in other living organisms. In short, bibliometric results highlight the current interest in DDR research in plants among DDR studies and can open new perspectives in the research field of DNA damage repair. Full article
(This article belongs to the Special Issue DNA Damage Responses in Plants)
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