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Programmed Induction of Endoreduplication by DNA Double-Strand Breaks in Arabidopsis

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Programmed Induction of Endoreduplication by DNA Double-Strand Breaks in Arabidopsis Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis Sumiko Adachia, Kazunori Minamisawaa, Yoko Okushimaa, Soichi Inagakia, Kaoru Yoshiyamaa, Youichi Kondoub, Eli Kaminumac, Mika Kawashimab, Tetsuro Toyodac, Minami Matsuib, Daisuke Kuriharad,e, Sachihiro Matsunagaf,g, and Masaaki Umedaa,1 aGraduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan; bPlant Science Center and cBioinformatics and Systems Engineering Division, Institute of Physical and Chemical Research (RIKEN), 1-7-22 Suehirocho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; dDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, Japan; eHigashiyama Live-Holonics Project, Japan Science and Technology Exploratory Research for Advanced Technology, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8602, Japan; fDepartment of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan; and gDepartment of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278-8510, Japan Edited* by Brian A. Larkins, University of Arizona, Tuscon, AZ, and approved May 4, 2011 (received for review March 8, 2011) Genome integrity is continuously threatened by external stresses orthologs, and knockout mutants show similar phenotypes to and endogenous hazards such as DNA replication errors and those of their mammalian counterparts. Arabidopsis atm mutants reactive oxygen species. The DNA damage checkpoint in meta- are sensitive to gamma radiation and are defective in transcrip- zoans ensures genome integrity by delaying cell-cycle progression tional induction of repair genes in response to irradiation (8). atr to repair damaged DNA or by inducing apoptosis. ATM and ATR mutants are sensitive to replication-blocking agents including (ataxia-telangiectasia-mutated and -Rad3-related) are sensor kinases HU and aphidicolin and to UVB light (9). However, it is note- that relay the damage signal to transducer kinases Chk1 and Chk2 worthy that, unlike mammalian ATR knockouts, Arabidopsis atr and to downstream cell-cycle regulators. Plants also possess ATM mutants are viable (9), suggesting that regulatory mechanisms and ATR orthologs but lack obvious counterparts of downstream underlying the DNA damage response are diverged between regulators. Instead, the plant-specific transcription factor SOG1 plants and animals. This result is not surprising because plants (suppressor of gamma response 1) plays a central role in the are continuously exposed to environmental stresses and thus transmission of signals from both ATM and ATR kinases. Here we need to deploy a robust checkpoint system to cope with geno- PLANT BIOLOGY show that in Arabidopsis, endoreduplication is induced by DNA toxic stress. Plants lack obvious counterparts of Cdc25, Chk1, double-strand breaks (DSBs), but not directly by DNA replication Chk2, p21, and p53. A recent report has identified a plant-specific stress. When root or sepal cells, or undifferentiated suspension transcription factor, SOG1 (suppressor of gamma response 1), cells, were treated with DSB inducers, they displayed increased that participates in pathways governed by both ATM and ATR cell size and DNA ploidy. We found that the ATM–SOG1 and kinases (10). In this study, we found that Arabidopsis cells treated ATR–SOG1 pathways both transmit DSB-derived signals and that with DSB inducers displayed increased cell size and DNA ploidy either one suffices for endocycle induction. These signaling path- without a concomitant change in chromosome number. This en- ways govern the expression of distinct sets of cell-cycle regulators, doreduplicative response required ATM, ATR, and SOG1, in- such as cyclin-dependent kinases and their suppressors. Our results dicating that it is a unique programmed mechanism for plants to demonstrate that Arabidopsis undergoes a programmed endore- survive under genotoxic stress. duplicative response to DSBs, suggesting that plants have evolved a distinct strategy to sustain growth under genotoxic stress. Results DSBs Cause Endoreduplication in Arabidopsis Root Tips and Sepals. root meristem | protein degradation To identify plant-specific mechanisms underlying the genotoxic stress response, we first observed Arabidopsis roots that had been amaged DNA needs to be repaired to prevent loss or in- exposed to the radiomimetic reagent zeocin (11, 12). When Dcorrect transmission of genetic information. Eukaryotic seedlings were transferred to 10-μM zeocin plates, root growth DNA damage checkpoints delay or arrest the cell cycle to pro- was arrested, and cyclin B1 expression (indicative of progression vide time for DNA repair before the cell enters a new round of into G2) was reduced (Fig. S1 A and B). AtGR1 and RAD51 DNA replication or mitosis (1). In metazoans, ATM and ATR transcripts were both strongly induced as early as 8 h after (ataxia-telangiectasia-mutated and -Rad3-related) are sensor ki- transfer to zeocin, consistent with activation of the known plant nases that play a crucial role in the checkpoint system. ATM transcriptional response to DSBs (Fig. S1C). Interestingly, the specifically responds to DNA double-strand breaks (DSBs), and epidermal cells of the root tip were enlarged by this treatment ATR primarily senses replication stress caused by a persistent (Fig. 1A). A plot of epidermal cell area against distance from the block of replication fork progression. ATM deficiency confers quiescent center (QC) at 24 h revealed that zeocin-induced cell > μ hypersensitivity to ionizing radiation (2), whereas ATR knockout expansion became pronounced in cells at distances of 150 m mutation is lethal (3, 4), and dominant-negative cell lines display hypersensitivity to UVB light, gamma radiation, hydroxyurea (HU), and aphidicolin (5, 6). ATM and ATR relay the damage Author contributions: S.A., K.M., M.M., D.K., S.M., and M.U. designed research; S.A., K.M., Y.O., K.Y., Y.K., E.K., M.K., T.T., D.K., and S.M. performed research; S.A., K.M., Y.O., S.I., signal to transducer kinases Chk2 and Chk1, respectively, which Y.K., E.K., M.K., T.T., D.K., S.M., and M.U. analyzed data; and S.A., Y.O., K.Y., E.K., S.M., then amplify the signal and regulate an overlapping set of sub- and M.U. wrote the paper. strates that trigger cell-cycle arrest and DNA repair (1). The The authors declare no conflict of interest. transcription factor p53, cyclin-dependent kinase (CDK) in- *This Direct Submission article had a prearranged editor. hibitor p21, and Cdc25 phosphatase are downstream regulators Data deposition: The microarray data reported in this paper have been deposited in the that control cell-cycle arrest in response to DNA damage. Center for Information Biology Gene Expression (CIBEX) database, http://cibex.nig.ac.jp/ Comparative sequence analyses among plants, yeast, and ani- (accession no. CBX148). mals indicate that some of the factors involved in DNA damage 1To whom correspondence should be addressed. E-mail: [email protected]. checkpoint and DSB repair systems are conserved between This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. vertebrates and plants (7). Plants also possess ATM and ATR 1073/pnas.1103584108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1103584108 PNAS Early Edition | 1of6 Downloaded by guest on September 24, 2021 This result indicates that zeocin induced cell expansion in the smaller dividing cells. Cell size usually correlates with nuclear DNA content (14); indeed, the percentage of 2C cells in zeocin-treated root tips was reduced, whereas that of 16C cells was increased (Fig. 1C). A similar but less pronounced effect of zeocin has also been noted in leaves (15). In root tips, the content of histone H2B- labeled DNA was elevated, especially in cells >150 μmfromthe QC (Fig. S3A), indicating that zeocin-induced cell enlargement is accompanied by an increase in DNA content, as observed during normal cell differentiation processes of Arabidopsis.The number of kinetochores, counted by marking the centromeric histone H3, was unaffected by zeocin (Fig. S3B), suggesting that the chromosome number did not change. These results indicate that zeocin treatment induced endoreduplication rather than endomitosis (in which cells enter but do not complete mitosis; ref. 16). Because endoreduplication rarely occurs in cells lo- cated <200 μm from the untreated QC (17), our results dem- onstrate that zeocin induces an early onset of endoreduplication in the root meristem. Gamma irradiation also enlarged Arabidopsis root cells (Fig. 1D). Because both zeocin and gamma rays induce DSBs, we then tested other genotoxic agents that induce replication blocks: HU, methyl methanesulfonate (MMS), cisplatin, and UV irradiation. Under conditions where root growth was retarded but not arrested (Fig. 1E), none of these agents induced cell expansion to the degree observed with zeocin and gamma radiation (Fig. 1D). Simultaneous application of zeocin and HU, but not zeocin and cisplatin, caused a partial inhibition (P = 0.017; Student t test) of cell expansion relative to zeocin treatment alone (Fig. S4A). Nevertheless, a significant cell enlargement still occurred with zeocin + HU relative to the nontreated control (Table S1), indicating that cells treated with HU retain their potential to undergo endoreduplication; the lack of significant difference in cell size
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