The Protein Arginine Methylase 5 (PRMT5/SKB1) Gene Is Required for the Maintenance of Root Stem Cells in Response to DNA Damage

Qiuling Li^a,
Yan Zhao^a,
Minghui Yue^{a, b},
Yongbiao Xue^{a, c},
Shilai Bao^{a
, ,}

a.
State Key Laboratory of Molecular and Developmental Biology, Center for Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b.
Graduate University of the Chinese Academy of Sciences, 19 Yuquan Road, Beijing 100039, China
c.
The State Key Laboratory of Plant Genomics, Center for Genome Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

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Corresponding author: E-mail address: slbao@genetics.ac.cn (Shilai Bao)

摘要

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Abstract: Plant root stem cells and their surrounding microenvironment, namely the stem cell niche, are hypersensitive to DNA damage. However, the molecular mechanisms that help maintain the genome stability of root stem cells remain elusive. Here we show that the root stem cells in the skb1 (Shk1 kinase binding protein 1) mutant undergoes DNA damage-induced cell death, which is enhanced when combined with a lesion of the Ataxia-telangiectasia mutated (ATM) or the ATM/RAD3-related (ATR) genes, suggesting that the SKB1 plays a synergistically effect with ATM and ATR in DNA damage pathway. We also provide evidence that SKB1 is required for the maintenance of quiescent center (QC), a root stem cell niche, under DNA damage treatments. Furthermore, we report decreased and ectopic expression of SHORTROOT (SHR) in response to DNA damage in the skb1 root tips, while the expression of SCARECROW (SCR) remains unaffected. Our results uncover a new mechanism of plant root stem cell maintenance under DNA damage conditions that requires SKB1.
- DNA damage /
- Root stem cells /
- QC maintenance

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参考文献(42)

[1]	Bao, S., Qyang, Y., Yang, P. et al. J. Biol. Chem., 276 (2001),pp. 14549-14552
[2]	Baurle, I., Laux, T. Apical meristems: the plant's fountain of youth Bioessays, 25 (2003),pp. 961-970
[3]	Bray, C.M., West, C.E. DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity New Phytol., 168 (2005),pp. 511-528
[4]	Colon-Carmona, A., You, R., Haimovitch-Gal, T. et al. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein Plant J., 20 (1999),pp. 503-508
[5]	Cruz-Ramirez, A., Diaz-Trivino, S., Blilou, I. et al. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division Cell, 150 (2012),pp. 1002-1015
[6]	Cui, H., Levesque, M.P., Vernoux, T. et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants Science, 316 (2007),pp. 421-425
[7]	Culligan, K., Tissier, A., Britt, A. Plant Cell, 16 (2004),pp. 1091-1104
[8]	Culligan, K.M., Robertson, C.E., Foreman, J. et al. ATR and ATM play both distinct and additive roles in response to ionizing radiation Plant J., 48 (2006),pp. 947-961
[9]	De Schutter, K., Joubes, J., Cools, T. et al. Plant Cell, 19 (2007),pp. 211-225
[10]	Deng, X., Gu, L., Liu, C. et al. Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 19114-19119
[11]	Dolan, L., Janmaat, K., Willemsen, V. et al. Development, 119 (1993),pp. 71-84
[12]	Flynn, R.L., Zou, L. ATR: a master conductor of cellular responses to DNA replication stress Trends Biochem. Sci., 36 (2010),pp. 133-140
[13]	Fulcher, N., Sablowski, R. Hypersensitivity to DNA damage in plant stem cell niches Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 20984-20988
[14]	Gilbreth, M., Yang, P., Bartholomeusz, G. et al. Negative regulation of mitosis in fission yeast by the Shk1 interacting protein Skb1 and its human homolog, Skb1Hs Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 14781-14786
[15]	Helariutta, Y., Fukaki, H., Wysocka-Diller, J. et al. Cell, 101 (2000),pp. 555-567
[16]	He, W., Ma, X., Yang, X. et al. A role for the arginine methylation of Rad9 in checkpoint control and cellular sensitivity to DNA damage Nucleic Acids Res., 39 (2011),pp. 4719-4727
[17]	Koc, A., Wheeler, L.J., Mathews, C.K. et al. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools J. Biol. Chem., 279 (2004),pp. 223-230
[18]	Koizumi, K., Gallagher, K.L. Identification of SHRUBBY, a SHORT-ROOT and SCARECROW interacting protein that controls root growth and radial patterning Development, 140 (2013),pp. 1292-1300
[19]	Koizumi, K., Hayashi, T., Wu, S. et al. The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 13010-13015
[20]	Lee, M.Y., Kim, M.A., Kim, H.J. et al. Alkylating agent methyl methanesulfonate (MMS) induces a wave of global protein hyperacetylation: implications in cancer cell death Biochem. Biophys. Res. Commun., 360 (2007),pp. 483-489
[21]	Levesque, M.P., Vernoux, T., Busch, W. et al. PLoS Biol., 4 (2006),p. e143
[22]	Li, Y., Zheng, L., Corke, F. et al. Genes Dev., 22 (2008),pp. 1331-1336
[23]	Menges, M., Hennig, L., Gruissem, W. et al. J. Biol. Chem., 277 (2002),pp. 41987-42002
[24]	Nakajima, K., Benfey, P.N. Signaling in and out: control of cell division and differentiation in the shoot and root Plant Cell, 14 (2002),pp. S265-S276
[25]	Nakajima, K., Sena, G., Nawy, T. et al. Intercellular movement of the putative transcription factor SHR in root patterning Nature, 413 (2001),pp. 307-311
[26]	Pal, S., Vishwanath, S.N., Erdjument-Bromage, H. et al. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes Mol. Cell. Biol., 24 (2004),pp. 9630-9645
[27]	Pei, Y., Niu, L., Lu, F. et al. Plant Physiol., 144 (2007),pp. 1913-1923
[28]	Ricaud, L., Proux, C., Renou, J.P. et al. PLoS One, 2 (2007),p. e430
[29]	Sabatini, S., Heidstra, R., Wildwater, M. et al. Genes Dev., 17 (2003),pp. 354-358
[30]	Sakano, K., Oikawa, S., Hasegawa, K. et al. Jpn J. Cancer Res., 92 (2001),pp. 1166-1174
[31]	Scoumanne, A., Zhang, J., Chen, X. PRMT5 is required for cell-cycle progression and p53 tumor suppressor function Nucleic Acids Res., 37 (2009),pp. 4965-4976
[32]	Shiloh, Y. The ATM-mediated DNA-damage response: taking shape Trends Biochem. Sci., 31 (2006),pp. 402-410
[33]	Tuteja, N., Ahmad, P., Panda, B.B. et al. Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases Mutat. Res., 681 (2009),pp. 134-149
[34]	Umeda, M., Umeda-Hara, C., Yamaguchi, M. et al. Differential expression of genes for cyclindependent protein kinases in rice plants Plant Physiol., 119 (1999),pp. 31-40
[35]	Wang, X., Zhang, Y., Ma, Q. et al. EMBO J., 26 (2007),pp. 1934-1941
[36]	Wildwater, M., Campilho, A., Perez-Perez, J.M. et al. Cell, 123 (2005),pp. 1337-1349
[37]	Williams, L., Fletcher, J.C. Curr. Opin. Plant Biol., 8 (2005),pp. 582-586
[38]	Wu, S., Gallagher, K.L. Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor Plant J., 74 (2013),pp. 148-159
[39]	Yang, M., Sun, J., Sun, X. et al. PLoS Genet., 5 (2009),p. e1000514
[40]	Yue, M., Li, Q., Zhang, Y. et al. Histone H4R3 methylation catalyzed by SKB1/PRMT5 is required for maintaining shoot apical meristem PLoS One, 8 (2013),p. e83258
[41]	Zhang, Z., Zhang, S., Zhang, Y. et al. Plant Cell, 23 (2011),pp. 396-411
[42]	Zhou, Z., Sun, X., Zou, Z. et al. PRMT5 regulates Golgi apparatus structure through methylation of the golgin GM130 Cell Res., 20 (2010),pp. 1023-1033