MDF is a conserved splicing factor and modulates cell division and stress response in Arabidopsis
Jazyk angličtina Země Spojené státy americké Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36265897
PubMed Central
PMC9585968
DOI
10.26508/lsa.202201507
PII: 6/1/e202201507
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis * genetika metabolismus MeSH
- buněčné dělení genetika MeSH
- lidé MeSH
- malý jaderný ribonukleoprotein U4-U6 genetika metabolismus MeSH
- malý jaderný ribonukleoprotein U5 * genetika metabolismus MeSH
- nestabilita genomu MeSH
- prekurzory RNA genetika metabolismus MeSH
- sestřihové faktory genetika MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- AT5G16780 protein, Arabidopsis MeSH Prohlížeč
- malý jaderný ribonukleoprotein U4-U6 MeSH
- malý jaderný ribonukleoprotein U5 * MeSH
- milk-derived factor MeSH Prohlížeč
- prekurzory RNA MeSH
- sestřihové faktory MeSH
The coordination of cell division with stress response is essential for maintaining genome stability in plant meristems. Proteins involved in pre-mRNA splicing are important for these processes in animal and human cells. Based on its homology to the splicing factor SART1, which is implicated in the control of cell division and genome stability in human cells, we analyzed if MDF has similar functions in plants. We found that MDF associates with U4/U6.U5 tri-snRNP proteins and is essential for correct splicing of 2,037 transcripts. Loss of MDF function leads to cell division defects and cell death in meristems and was associated with up-regulation of stress-induced genes and down-regulation of mitotic regulators. In addition, the mdf-1 mutant is hypersensitive to DNA damage treatment supporting its role in coordinating stress response with cell division. Our analysis of a dephosphomutant of MDF suggested how its protein activity might be controlled. Our work uncovers the conserved function of a plant splicing factor and provides novel insight into the interplay of pre-mRNA processing and genome stability in plants.
Institute of Microbiology of the Czech Academy of Sciences Prague Czech Republic
Institute of Plant Sciences and Microbiology University of Hamburg Hamburg Germany
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Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, Kondou Y, Kaminuma E, Kawashima M, Toyoda T, Matsui M, et al. (2011) Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci U S A 108: 10004–10009. 10.1073/pnas.1103584108 PubMed DOI PMC
Albaqami M, Laluk K, Reddy ASN (2019) The Arabidopsis splicing regulator SR45 confers salt tolerance in a splice isoform-dependent manner. Plant Mol Biol 100: 379–390. 10.1007/s11103-019-00864-4 PubMed DOI
Ali GS, Palusa SG, Golovkin M, Prasad J, Manley JL, Reddy AS (2007) Regulation of plant developmental processes by a novel splicing factor. PLoS One 2: e471. 10.1371/journal.pone.0000471 PubMed DOI PMC
Ali GS, Prasad KVSK, Hanumappa M, Reddy ASN (2008) Analyses of in vivo interaction and mobility of two spliceosomal proteins using FRAP and BiFC. PLoS One 3: e1953. 10.1371/journal.pone.0001953 PubMed DOI PMC
Allen WL, Stevenson L, Coyle VM, Jithesh PV, Proutski I, Carson G, Gordon MA, Lenz HJD, Van Schaeybroeck S, Longley DB, et al. (2012) A systems biology approach identifies SART1 as a novel determinant of both 5-fluorouracil and SN38 drug resistance in colorectal cancer. Mol Cancer Ther 11: 119–131. 10.1158/1535-7163.mct-11-0510 PubMed DOI PMC
Bazin J, Mariappan K, Jiang Y, Blein T, Voelz R, Crespi M, Hirt H (2020) Role of MPK4 in pathogen-associated molecular pattern-triggered alternative splicing in Arabidopsis. PLoS Pathog 16: e1008401. 10.1371/journal.ppat.1008401 PubMed DOI PMC
Beggs JD (2005) Lsm proteins and RNA processing. Biochem Soc Trans 33: 433–438. 10.1042/bst0330433 PubMed DOI
Bessonov S, Anokhina M, Will CL, Urlaub H, Luhrmann R (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846–850. 10.1038/nature06842 PubMed DOI
Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2009) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152: 166–176. 10.1104/pp.109.149930 PubMed DOI PMC
Blencowe BJ, Bowman JA, McCracken S, Rosonina E (1999) SR-related proteins and the processing of messenger RNA precursors. Biochem Cell Biol 77: 277–291. 10.1139/o99-048 PubMed DOI
Boucas J, Riabinska A, Jokic M, Herter-Sprie GS, Chen S, Hopker K, Reinhardt HC (2012) Posttranscriptional regulation of gene expression-adding another layer of complexity to the DNA damage response. Front Genet 3: 159. 10.3389/fgene.2012.00159 PubMed DOI PMC
Bourbousse C, Vegesna N, Law JA (2018) SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis. Proc Natl Acad Sci U S A 115: E12453–E12462. 10.1073/pnas.1810582115 PubMed DOI PMC
Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G (2004) GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710–3715. 10.1093/bioinformatics/bth456 PubMed DOI PMC
Carrasco-Lopez C, Hernandez-Verdeja T, Perea-Resa C, Abia D, Catala R, Salinas J (2017) Environment-dependent regulation of spliceosome activity by the LSM2-8 complex in Arabidopsis. Nucleic Acids Res 45: 7416–7431. 10.1093/nar/gkx375 PubMed DOI PMC
Carvalho RF, Carvalho SD, Duque P (2010) The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol 154: 772–783. 10.1104/pp.110.155523 PubMed DOI PMC
Carvalho RF, Szakonyi D, Simpson CG, Barbosa IC, Brown JW, Baena-Gonzalez E, Duque P (2016) The Arabidopsis SR45 splicing factor, a negative regulator of sugar signaling, modulates SNF1-related protein kinase 1 stability. Plant Cell 28: 1910–1925. 10.1105/tpc.16.00301 PubMed DOI PMC
Casson SA, Topping JF, Lindsey K (2009) MERISTEM-DEFECTIVE, an RS domain protein, is required for the correct meristem patterning and function in Arabidopsis. Plant J 57: 857–869. 10.1111/j.1365-313x.2008.03738.x PubMed DOI
Chen SL, Rooney TJ, Hu AR, Beard HS, Garrett WM, Mangalath LM, Powers JJ, Cooper B, Zhang XN (2019) Quantitative proteomics reveals a role for SERINE/ARGININE-Rich 45 in regulating RNA metabolism and modulating transcriptional suppression via the ASAP complex in Arabidopsis thaliana. Front Plant Sci 10: 1116. 10.3389/fpls.2019.01116 PubMed DOI PMC
Clough SJ, Bent AF (1998) Floral dip: A simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10.1046/j.1365-313x.1998.00343.x PubMed DOI
Culligan KM, Robertson CE, Foreman J, Doerner P, Britt AB (2006) ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J 48: 947–961. 10.1111/j.1365-313x.2006.02931.x PubMed DOI
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469. 10.1104/pp.103.027979 PubMed DOI PMC
de la Fuente van Bentem S, Anrather D, Roitinger E, Djamei A, Hufnagl T, Barta A, Csaszar E, Dohnal I, Lecourieux D, Hirt H (2006) Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Res 34: 3267–3278. 10.1093/nar/gkl429 PubMed DOI PMC
Dutertre M, Sanchez G, Barbier J, Corcos L, Auboeuf D (2011) The emerging role of pre-messenger RNA splicing in stress responses: Sending alternative messages and silent messengers. RNA Biol 8: 740–747. 10.4161/rna.8.5.16016 PubMed DOI
Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20: 45–58. 10.1101/gr.093302.109 PubMed DOI PMC
Fukumura K, Inoue K, Mayeda A (2018) Splicing activator RNPS1 suppresses errors in pre-mRNA splicing: A key factor for mRNA quality control. Biochem Biophys Res Commun 496: 921–926. 10.1016/j.bbrc.2018.01.120 PubMed DOI
Furukawa T, Curtis MJ, Tominey CM, Duong YH, Wilcox BW, Aggoune D, Hays JB, Britt AB (2010) A shared DNA-damage-response pathway for induction of stem-cell death by UVB and by gamma irradiation. DNA Repair (Amst) 9: 940–948. 10.1016/j.dnarep.2010.06.006 PubMed DOI
Garcia V, Bruchet H, Camescasse D, Granier F, Bouchez D, Tissier A (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15: 119–132. 10.1105/tpc.006577 PubMed DOI PMC
Gietz RD, Triggs-Raine B, Robbins A, Graham KC, Woods RA (1997) Identification of proteins that interact with a protein of interest: Applications of the yeast two-hybrid system. Mol Cell Biochem 172: 67–79. PubMed
Gottschalk A, Neubauer G, Banroques J, Mann M, Luhrmann R, Fabrizio P (1999) Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6middle dotU5] tri-snRNP. EMBO J 18: 4535–4548. 10.1093/emboj/18.16.4535 PubMed DOI PMC
Hacker I, Sander B, Golas MM, Wolf E, Karagoz E, Kastner B, Stark H, Fabrizio P, Luhrmann R (2008) Localization of Prp8, Brr2, Snu114 and U4/U6 proteins in the yeast tri-snRNP by electron microscopy. Nat Struct Mol Biol 15: 1206–1212. 10.1038/nsmb.1506 PubMed DOI
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: R19. 10.1186/gb-2007-8-2-r19 PubMed DOI PMC
Horvath BM, Kourova H, Nagy S, Nemeth E, Magyar Z, Papdi C, Ahmad Z, Sanchez-Perez GF, Perilli S, Blilou I, et al. (2017) Arabidopsis RETINOBLASTOMA RELATED directly regulates DNA damage responses through functions beyond cell cycle control. EMBO J 36: 1261–1278. 10.15252/embj.201694561 PubMed DOI PMC
Hosokawa M, Kadota R, Shichijo S, Itoh K, Dmitriev I, Krasnykh V, Curiel DT, Takue Y, Wakasugi H, Takashima S, et al. (2005) Cell cycle arrest and apoptosis induced by SART-1 gene transduction. Anticancer Res 25: 1983–1990. PubMed
Hu Z, Cools T, De Veylder L (2016) Mechanisms used by plants to cope with DNA damage. Annu Rev Plant Biol 67: 439–462. 10.1146/annurev-arplant-043015-111902 PubMed DOI
Huang Y, Steitz JA (2005) SRprises along a messenger[R8S2Q1M7]s journey. Mol Cell 17: 613–615. 10.1016/j.molcel.2005.02.020 PubMed DOI
Johnson RA, Conklin PA, Tjahjadi M, Missirian V, Toal T, Brady SM, Britt AB (2018) SUPPRESSOR of GAMMA RESPONSE1 links DNA damage response to organ regeneration. Plant Physiol 176: 1665–1675. 10.1104/pp.17.01274 PubMed DOI PMC
Kall L, Canterbury JD, Weston J, Noble WS, MacCoss MJ (2007) Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods 4: 923–925. 10.1038/nmeth1113 PubMed DOI
Kallai BM, Kourova H, Chumova J, Papdi C, Trogelova L, Kofronova O, Hozak P, Filimonenko V, Meszaros T, Magyar Z, et al. (2020) γ-Tubulin interacts with E2F transcription factors to regulate proliferation and endocycling in Arabidopsis. J Exp Bot 71: 1265–1277. 10.1093/jxb/erz498 PubMed DOI
Kanno T, Venhuizen P, Wen TN, Lin WD, Chiou P, Kalyna M, Matzke AJM, Matzke M (2018) PRP4KA, a putative spliceosomal protein kinase, is important for alternative splicing and development in Arabidopsis thaliana. Genetics 210: 1267–1285. 10.1534/genetics.118.301515 PubMed DOI PMC
Kikuchi M, Nakao M, Inoue Y, Matsunaga K, Shichijo S, Yamana H, Itoh K (1999) Identification of a SART-1-derived peptide capable of inducing HLA-A24-restricted and tumor-specific cytotoxic T lymphocytes. Int J Cancer 81: 459–466. 10.1002/(sici)1097-0215(19990505)81:3<459::aid-ijc21>3.0.co;2-6 PubMed DOI
Kim GD, Cho YH, Lee BH, Yoo SD (2017) STABILIZED1 modulates pre-mRNA splicing for thermotolerance. Plant Physiol 173: 2370–2382. 10.1104/pp.16.01928 PubMed DOI PMC
Kittler R, Putz G, Pelletier L, Poser I, Heninger AK, Drechsel D, Fischer S, Konstantinova I, Habermann B, Grabner H, et al. (2004) An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division. Nature 432: 1036–1040. 10.1038/nature03159 PubMed DOI
Koncz C, Dejong F, Villacorta N, Szakonyi D, Koncz Z (2012) The spliceosome-activating complex: Molecular mechanisms underlying the function of a pleiotropic regulator. Front Plant Sci 3: 9. 10.3389/fpls.2012.00009 PubMed DOI PMC
Laloum T, Martin G, Duque P (2018) Alternative splicing control of abiotic stress responses. Trends Plant Sci 23: 140–150. 10.1016/j.tplants.2017.09.019 PubMed DOI
Li X, Niu T, Manley JL (2007) The RNA binding protein RNPS1 alleviates ASF/SF2 depletion-induced genomic instability. RNA 13: 2108–2115. 10.1261/rna.734407 PubMed DOI PMC
Ling Y, Mahfouz MM, Zhou S (2021) Pre-mRNA alternative splicing as a modulator for heat stress response in plants. Trends Plant Sci 26: 1153–1170. 10.1016/j.tplants.2021.07.008 PubMed DOI
Liu S, Rauhut R, Vornlocher HP, Luhrmann R (2006) The network of protein-protein interactions within the human U4/U6.U5 tri-snRNP. RNA 12: 1418–1430. 10.1261/rna.55406 PubMed DOI PMC
Locascio A, Blázquez MA, Alabadí D (2013) Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 23: 804–809. 10.1016/j.cub.2013.03.053 PubMed DOI
Lv B, Hu K, Tian T, Wei K, Zhang F, Jia Y, Tian H, Ding Z (2021) The pre-mRNA splicing factor RDM16 regulates root stem cell maintenance in Arabidopsis. J Integr Plant Biol 63: 662–678. 10.1111/jipb.13006 PubMed DOI
Mahrez W, Shin J, Munoz-Viana R, Figueiredo DD, Trejo-Arellano MS, Exner V, Siretskiy A, Gruissem W, Kohler C, Hennig L (2016) BRR2a affects flowering time via FLC splicing. PLoS Genet 12: e1005924. 10.1371/journal.pgen.1005924 PubMed DOI PMC
Makarova OV, Makarov EM, Luhrmann R (2001) The 65 and 110 kDa SR-related proteins of the U4/U6.U5 tri-snRNP are essential for the assembly of mature spliceosomes. EMBO J 20: 2553–2563. 10.1093/emboj/20.10.2553 PubMed DOI PMC
Martin G, Marquez Y, Mantica F, Duque P, Irimia M (2021) Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals. Genome Biol 22: 35. 10.1186/s13059-020-02258-y PubMed DOI PMC
Neugebauer KM, Stolk JA, Roth MB (1995) A conserved epitope on a subset of SR proteins defines a larger family of pre-mRNA splicing factors. J Cell Biol 129: 899–908. 10.1083/jcb.129.4.899 PubMed DOI PMC
Nguyen THD, Galej WP, Bai XC, Oubridge C, Newman AJ, Scheres SHW, Nagai K (2016) Cryo-EM structure of the yeast U4/U6.U5 tri-snRNP at 3.7 Å resolution. Nature 530: 298–302. 10.1038/nature16940 PubMed DOI PMC
Nimeth BA, Riegler S, Kalyna M (2020) Alternative splicing and DNA damage response in plants. Front Plant Sci 11: 91. 10.3389/fpls.2020.00091 PubMed DOI PMC
Nisa MU, Huang Y, Benhamed M, Raynaud C (2019) The plant DNA damage response: Signaling pathways leading to growth inhibition and putative role in response to stress conditions. Front Plant Sci 10: 653. 10.3389/fpls.2019.00653 PubMed DOI PMC
Ogita N, Okushima Y, Tokizawa M, Yamamoto YY, Tanaka M, Seki M, Makita Y, Matsui M, Okamoto-Yoshiyama K, Sakamoto T, et al. (2018) Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis. Plant J 94: 439–453. 10.1111/tpj.13866 PubMed DOI
Perea-Resa C, Hernandez-Verdeja T, Lopez-Cobollo R, Castellano MdM, Salinas J (2012) LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell 24: 4930–4947. 10.1105/tpc.112.103697 PubMed DOI PMC
Roitinger E, Hofer M, Kocher T, Pichler P, Novatchkova M, Yang J, Schlogelhofer P, Mechtler K (2015) Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol Cell Proteomics 14: 556–571. 10.1074/mcp.m114.040352 PubMed DOI PMC
Shimotohno A, Aki SS, Takahashi N, Umeda M (2021) Regulation of the plant cell cycle in response to hormones and the environment. Annu Rev Plant Biol 72: 273–296. 10.1146/annurev-arplant-080720-103739 PubMed DOI
Sjogren CA, Bolaris SC, Larsen PB (2015) Aluminum-dependent terminal differentiation of the Arabidopsis root tip is mediated through an ATR-ALT2-and SOG1-regulated transcriptional response. Plant Cell 27: 2501–2515. 10.1105/tpc.15.00172 PubMed DOI PMC
Stevens SW, Abelson J (1999) Purification of the yeast U4/U6.U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc Natl Acad Sci U S A 96: 7226–7231. 10.1073/pnas.96.13.7226 PubMed DOI PMC
Takahashi N, Ogita N, Takahashi T, Taniguchi S, Tanaka M, Seki M, Umeda M (2019) A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. Elife 8: e43944. 10.7554/elife.43944 PubMed DOI PMC
Tharun S (2009) Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int Rev Cell Mol Biol 272: 149–189. 10.1016/S1937-6448(08)01604-3 PubMed DOI
van Nues RW, Beggs JD (2001) Functional contacts with a range of splicing proteins suggest a central role for Brr2p in the dynamic control of the order of events in spliceosomes of Saccharomyces cerevisiae. Genetics 157: 1451–1467. 10.1093/genetics/157.4.1451 PubMed DOI PMC
Wan R, Bai R, Zhan X, Shi Y (2020) How is precursor messenger RNA spliced by the spliceosome? Annu Rev Biochem 89: 333–358. 10.1146/annurev-biochem-013118-111024 PubMed DOI
Wan R, Yan C, Bai R, Wang L, Huang M, Wong CCL, Shi Y (2016) The 3.8 Å structure of the U4/U6.U5 tri-snRNP: Insights into spliceosome assembly and catalysis. Science 351: 466–475. 10.1126/science.aad6466 PubMed DOI
Wang L, Zhan L, Zhao Y, Huang Y, Wu C, Pan T, Qin Q, Xu Y, Deng Z, Li J, et al. (2021) The ATR-WEE1 kinase module inhibits the MAC complex to regulate replication stress response. Nucleic Acids Res 49: 1411–1425. 10.1093/nar/gkaa1082 PubMed DOI PMC
Waterworth WM, Wilson M, Wang D, Nuhse T, Warward S, Selley J, West CE (2019) Phosphoproteomic analysis reveals plant DNA damage signalling pathways with a functional role for histone H2AX phosphorylation in plant growth under genotoxic stress. Plant J 100: 1007–1021. 10.1111/tpj.14495 PubMed DOI PMC
Wilkinson ME, Charenton C, Nagai K (2020) RNA splicing by the spliceosome. Annu Rev Biochem 89: 359–388. 10.1146/annurev-biochem-091719-064225 PubMed DOI
Will CL, Luhrmann R (2011) Spliceosome structure and function. Cold Spring Harb Perspect Biol 3: a003707. 10.1101/cshperspect.a003707 PubMed DOI PMC
Yi D, Alvim Kamei CL, Cools T, Vanderauwera S, Takahashi N, Okushima Y, Eekhout T, Yoshiyama KO, Larkin J, Van den Daele H, et al. (2014) The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. Plant Cell 26: 296–309. 10.1105/tpc.113.118943 PubMed DOI PMC
Yildirim A, Mozaffari-Jovin S, Wallisch AK, Schafer J, Ludwig SEJ, Urlaub H, Luhrmann R, Wolfrum U (2021) SANS (USH1G) regulates pre-mRNA splicing by mediating the intra-nuclear transfer of tri-snRNP complexes. Nucleic Acids Res 49: 5845–5866. 10.1093/nar/gkab386 PubMed DOI PMC
Yoshiyama K, Conklin PA, Huefner ND, Britt AB (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc Natl Acad Sci U S A 106: 12843–12848. 10.1073/pnas.0810304106 PubMed DOI PMC
Yoshiyama KO, Aoshima N, Takahashi N, Sakamoto T, Hiruma K, Saijo Y, Hidema J, Umeda M, Kimura S (2020) SUPPRESSOR OF GAMMA RESPONSE 1 acts as a regulator coordinating crosstalk between DNA damage response and immune response in Arabidopsis thaliana. Plant Mol Biol 103: 321–340. 10.1007/s11103-020-00994-0 PubMed DOI
Yoshiyama KO, Kobayashi J, Ogita N, Ueda M, Kimura S, Maki H, Umeda M (2013. a) ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis. EMBO Rep 14: 817–822. 10.1038/embor.2013.112 PubMed DOI PMC
Yoshiyama KO, Sakaguchi K, Kimura S (2013. b) DNA damage response in plants: Conserved and variable response compared to animals. Biology (Basel) 2: 1338–1356. 10.3390/biology2041338 PubMed DOI PMC