Genome-wide and molecular characterization of the DNA replication helicase 2 (DNA2) gene family in rice under drought and salt stress

Rice plants experience various biotic (such as insect and pest attack) and abiotic (such as drought, salt, heat, and cold etc.) stresses during the growing season, resulting in DNA damage and the subsequent losses in rice production. DNA Replication Helicase/Nuclease2 (DNA2) is known to be involved in DNA replication and repair. In animals and yeast DNA2 are well characterized because it has the abilities of both helicase and nuclease, it plays a crucial role in DNA replication in the nucleus and mitochondrial genomes. However; they are not fully examined in plants due to less focused on plants damage repair. To fill this research gap, the current study focused on the genome-wide identification and characterization of OsDNA2 genes, along with analyses of their transcriptional expression, duplication, and phylogeny in rice. Overall, 17 OsDNA2 members were reported to be found on eight different chromosomes (2, 3, 4, 6, 7, 9, 10, and 11). Among these chromosomes (Chr), Chr4 contained a maximum of six OsDNA2 genes. Based on phylogenetic analysis, the OsDNA2 gene members were clustered into three different groups. Furthermore, the conserved domains, gene structures, and cis-regulatory elements were systematically investigated. Gene duplication analysis revealed that OsDNA2_2 had an evolutionary relationship with OsDNA2_14, OsDNA2_5 with OsDNA2_6, and OsDNA2_1 with OsDNA2_8. Moreover, results showed that the conserved domain (AAA_11 superfamily) were present in the OsDNA2 genes, which belongs to the DEAD-like helicase superfamily. In addition, to understand the post-transcriptional modification of OsDNA2 genes, miRNAs were predicted, where 653 miRNAs were reported to target 17 OsDNA2 genes. The results indicated that at the maximum, OsDNA2_1 and OsDNA2_4 were targeted by 74 miRNAs each, and OsDNA2_9 was less targeted (20 miRNAs). The three-dimensional (3D) structures of 17 OsDNA2 proteins were also predicted. Expression of OsDNA2 members was also carried out under drought and salt stresses, and conclusively their induction indicated the possible involvement of OsDNA2 in DNA repair under stress when compared with the control. Further studies are recommended to confirm where this study will offer valuable basic data on the functioning of DNA2 genes in rice and other crop plants.

[1]  S. Nanda,et al.  Genome-wide identification and expression analysis of CRK gene family in chili pepper (Capsicum annuum L.) in response to Colletotrichum truncatum infection , 2022, The Journal of Horticultural Science and Biotechnology.

[2]  R. Varshney,et al.  Smart reprograming of plants against salinity stress using modern biotechnological tools , 2022, Critical reviews in biotechnology.

[3]  Obaid ur Rehman,et al.  Genome-Wide Identification and Characterization of Receptor-Like Protein Kinase 1 (RPK1) Gene Family in Triticum aestivum Under Drought Stress , 2022, Frontiers in Genetics.

[4]  An Yan,et al.  Positional cues and cell division dynamics drive meristem development and archegonium formation in Ceratopteris gametophytes , 2022, Communications Biology.

[5]  Obaid ur Rehman,et al.  Role of the Type-B Authentic Response Regulator Gene Family in Fragrant Rice under Alkaline-salt Stress. , 2022, Physiologia plantarum.

[6]  Vinod,et al.  Genome-Wide Identification and Expression Analysis of the Thioredoxin (Trx) Gene Family Reveals Its Role in Leaf Rust Resistance in Wheat (Triticum aestivum L.) , 2022, Frontiers in Genetics.

[7]  B. Courtois,et al.  Integrative Approach for Precise Genotyping and Transcriptomics of Salt Tolerant Introgression Rice Lines , 2022, Frontiers in Plant Science.

[8]  A. Afroz,et al.  Phenylalanine Ammonia-Lyase (PAL) Genes Family in Wheat (Triticum aestivum L.): Genome-Wide Characterization and Expression Profiling , 2021, Agronomy.

[9]  K. Wabnik,et al.  Shaping the Organ: A Biologist Guide to Quantitative Models of Plant Morphogenesis , 2021, Frontiers in Plant Science.

[10]  A. Raza,et al.  Genome-Wide Analysis and Expression Profile of Superoxide Dismutase (SOD) Gene Family in Rapeseed (Brassica napus L.) under Different Hormones and Abiotic Stress Conditions , 2021, Antioxidants.

[11]  Qing Li,et al.  Rtt105 promotes high-fidelity DNA replication and repair by regulating the single-stranded DNA-binding factor RPA , 2021, Proceedings of the National Academy of Sciences.

[12]  Ulrich Rass,et al.  DNA2 in Chromosome Stability and Cell Survival—Is It All about Replication Forks? , 2021, International journal of molecular sciences.

[13]  Xueyong Li,et al.  Narrow Leaf21, Encoding Ribosomal Protein RPS3A, Controls Leaf Development in Rice. , 2021, Plant physiology.

[14]  P. Robbins,et al.  DNA damage—how and why we age? , 2021, eLife.

[15]  Silvio C. E. Tosatto,et al.  The InterPro protein families and domains database: 20 years on , 2020, Nucleic Acids Res..

[16]  A. Kohli,et al.  Comparative Transcriptomics and Co-Expression Networks Reveal Tissue- and Genotype-Specific Responses of qDTYs to Reproductive-Stage Drought Stress in Rice (Oryza sativa L.) , 2020, Genes.

[17]  G. Yadav,et al.  Structural Aspects of DNA Repair and Recombination in Crop Improvement , 2020, Frontiers in Genetics.

[18]  He Yi-qin,et al.  Genome‐wide analysis of ethylene‐insensitive3 (EIN3/EIL) in Triticum aestivum , 2020 .

[19]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[20]  J. Vertemara,et al.  Functional and structural insights into the MRX/MRN complex, a key player in recognition and repair of DNA double-strand breaks , 2020, Computational and structural biotechnology journal.

[21]  S. Bunting,et al.  The Regulation of Homologous Recombination by Helicases , 2020, Genes.

[22]  Xigang Liu,et al.  Same Actor in Different Stages: Genes in Shoot Apical Meristem Maintenance and Floral Meristem Determinacy in Arabidopsis , 2020, Frontiers in Ecology and Evolution.

[23]  A. Millar.  The Function of miRNAs in Plants , 2020, Plants.

[24]  Judith L. Campbell,et al.  Multiple roles of DNA2 nuclease/helicase in DNA metabolism, genome stability and human diseases , 2019, Nucleic acids research.

[25]  B. Shen,et al.  TRAF6 mediates human DNA2 polyubiquitination and nuclear localization to maintain nuclear genome integrity , 2019, Nucleic acids research.

[26]  C. Raynaud,et al.  The Plant DNA Damage Response: Signaling Pathways Leading to Growth Inhibition and Putative Role in Response to Stress Conditions , 2019, Front. Plant Sci..

[27]  J. Traas.  Organogenesis at the Shoot Apical Meristem , 2018, Plants.

[28]  Julie Bianchi,et al.  PrimPol is required for the maintenance of efficient nuclear and mitochondrial DNA replication in human cells , 2018, bioRxiv.

[29]  A. Carr,et al.  Preserving replication fork integrity and competence via the homologous recombination pathway , 2018, DNA repair.

[30]  M. Longhese,et al.  Processing of DNA Ends in the Maintenance of Genome Stability , 2018, Front. Genet..

[31]  Xiuren Zhang,et al.  Genome-Wide Investigation of the Role of MicroRNAs in Desiccation Tolerance in the Resurrection Grass Tripogon loliiformis , 2018, Plants.

[32]  Torsten Schwede,et al.  SWISS-MODEL: homology modelling of protein structures and complexes , 2018, Nucleic Acids Res..

[33]  Hongyu Wu,et al.  Identification and expression of GRAS family genes in maize (Zea mays L.) , 2017, PloS one.

[34]  J. Błasiak,et al.  DNA2—An Important Player in DNA Damage Response or Just Another DNA Maintenance Protein? , 2017, International journal of molecular sciences.

[35]  Baohua Wang,et al.  Identification of Salt Tolerance-related microRNAs and Their Targets in Maize (Zea mays L.) Using High-throughput Sequencing and Degradome Analysis , 2017, Front. Plant Sci..

[36]  G. Walker,et al.  Mechanisms of DNA damage, repair, and mutagenesis , 2017, Environmental and molecular mutagenesis.

[37]  L. Symington,et al.  RPA Stabilization of Single-Stranded DNA Is Critical for Break-Induced Replication. , 2016, Cell reports.

[38]  C. Foyer,et al.  Intracellular Redox Compartmentation and ROS-Related Communication in Regulation and Signaling1[OPEN] , 2016, Plant Physiology.

[39]  Ning Jia,et al.  A DNA2 Homolog Is Required for DNA Damage Repair, Cell Cycle Regulation, and Meristem Maintenance in Plants1[OPEN] , 2016, Plant Physiology.

[40]  N. Pavletich,et al.  Dna2 nuclease-helicase structure, mechanism and regulation by Rpa , 2015, eLife.

[41]  P. Cejka,et al.  The Saccharomyces cerevisiae Dna2 can function as a sole nuclease in the processing of Okazaki fragments in DNA replication , 2015, Nucleic acids research.

[42]  M. Whitby,et al.  Recombination occurs within minutes of replication blockage by RTS1 producing restarted forks that are prone to collapse , 2015, eLife.

[43]  N. Tuteja,et al.  DNA Damage and Repair in Plants under Ultraviolet and Ionizing Radiations , 2015, TheScientificWorldJournal.

[44]  Radhakrishnan Kanagaraj,et al.  DNA2 Cooperates with the WRN and BLM RecQ Helicases to Mediate Long-range DNA End Resection in Human Cells* , 2014, The Journal of Biological Chemistry.

[45]  Jenn-Kang Hwang,et al.  CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation , 2014, PloS one.

[46]  V. Bohr,et al.  Human RecQ helicases in DNA repair, recombination, and replication. , 2014, Annual review of biochemistry.

[47]  A. Widmer,et al.  Genome-wide Comparative Analysis of the GRAS Gene Family in Populus, Arabidopsis and Rice , 2014, Plant Molecular Biology Reporter.

[48]  K. Raney,et al.  Structure and Mechanisms of SF1 DNA Helicases. , 2013, Advances in experimental medicine and biology.

[49]  K. Raney,et al.  Structure and Mechanisms of SF1 DNA Helicases. , 2013, Advances in experimental medicine and biology.

[50]  B. Liu,et al.  The Arabidopsis At1g30680 gene encodes a homologue to the phage T7 gp4 protein that has both DNA primase and DNA helicase activities , 2013, BMC Plant Biology.

[51]  C. Godin,et al.  Systems Analysis of Shoot Apical Meristem Growth and Development: Integrating Hormonal and Mechanical Signaling , 2012, Plant Cell.

[52]  L. Aravind,et al.  Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms , 2012, Bioinform..

[53]  R. Gredilla,et al.  Nuclear and Mitochondrial DNA Repair in Selected Eukaryotic Aging Model Systems , 2012, Oxidative medicine and cellular longevity.

[54]  Yuliang Wu.  Unwinding and Rewinding: Double Faces of Helicase? , 2012, Journal of nucleic acids.

[55]  G. Giglia-Mari,et al.  Kinetics of endogenous mouse FEN1 in base excision repair , 2012, Nucleic acids research.

[56]  Olga Golosova,et al.  Unipro UGENE: a unified bioinformatics toolkit , 2012, Bioinform..

[57]  Peer Bork,et al.  SMART 7: recent updates to the protein domain annotation resource , 2011, Nucleic Acids Res..

[58]  A. Kuzminov.  Homologous Recombination—Experimental Systems, Analysis, and Significance , 2011, EcoSal Plus.

[59]  B. Wold,et al.  Inviability of a DNA2 deletion mutant is due to the DNA damage checkpoint , 2011, Cell cycle.

[60]  B. Shen,et al.  Okazaki fragment maturation: nucleases take centre stage. , 2011, Journal of molecular cell biology.

[61]  S. Kowalczykowski,et al.  DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2 , 2010, Nature.

[62]  Young-Hoon Kang,et al.  Dna2 on the road to Okazaki fragment processing and genome stability in eukaryotes , 2010, Critical reviews in biochemistry and molecular biology.

[63]  S. Stewart,et al.  Human Dna2 Is a Nuclear and Mitochondrial DNA Maintenance Protein , 2009, Molecular and Cellular Biology.

[64]  Mikael Bodén,et al.  MEME Suite: tools for motif discovery and searching , 2009, Nucleic Acids Res..

[65]  D. Bogenhagen,et al.  Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates and defective in myopathy , 2008, Molecular cell.

[66]  Wolf-Dietrich Heyer,et al.  Homologous recombination in DNA repair and DNA damage tolerance , 2008, Cell Research.

[67]  Guo-Min Li,et al.  Mechanisms and functions of DNA mismatch repair , 2008, Cell Research.

[68]  An-Yuan Guo,et al.  [GSDS: a gene structure display server]. , 2007, Yi chuan = Hereditas.

[69]  J. Groden,et al.  The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. , 2006, Biochemistry.

[70]  I. Hickson,et al.  DNA helicases required for homologous recombination and repair of damaged replication forks. , 2006, Annual review of genetics.

[71]  Z. Xiang,et al.  Advances in homology protein structure modeling. , 2006, Current protein & peptide science.

[72]  Judith L. Campbell,et al.  Biochemical analysis of human Dna2 , 2006, Nucleic acids research.

[73]  Z. Weng,et al.  Main‐chain conformational tendencies of amino acids , 2005, Proteins.

[74]  J. Shampay,et al.  New temperature-sensitive mutants of Saccharomyces cerevisiae affecting DNA replication , 2004, Molecular and General Genetics MGG.

[75]  Ron D. Appel,et al.  ExPASy: the proteomics server for in-depth protein knowledge and analysis , 2003, Nucleic Acids Res..

[76]  F. B. Pickett,et al.  Splitting pairs: the diverging fates of duplicated genes , 2002, Nature Reviews Genetics.

[77]  Jung-Ae Kim,et al.  Tripartite structure of Saccharomyces cerevisiae Dna2 helicase/endonuclease. , 2001, Nucleic acids research.

[78]  Judith L Campbell,et al.  The Nuclease Activity of the Yeast Dna2 Protein, Which Is Related to the RecB-like Nucleases, Is Essential in Vivo * , 2000, The Journal of Biological Chemistry.

[79]  Judith L Campbell,et al.  A yeast replicative helicase, Dna2 helicase, interacts with yeast FEN-1 nuclease in carrying out its essential function , 1997, Molecular and cellular biology.