SUPPRESSOR OF GAMMA RESPONSE1 Links DNA Damage Response to Organ Regeneration

Overview

Journal Plant Physiol

Specialty Physiology

Date 2017 Dec 10

PMID 29222192

Citations 25

Authors

Ross A Johnson

Phillip A Conklin

Michelle Tjahjadi

Victor Missirian

Ted Toal

Siobhan M Brady

Anne B Britt

Affiliations

Soon will be listed here.

Abstract

In Arabidopsis, DNA damage-induced programmed cell death is limited to the meristematic stem cell niche and its early descendants. The significance of this cell-type-specific programmed cell death is unclear. Here, we demonstrate in roots that it is the programmed destruction of the mitotically compromised stem cell niche that triggers its regeneration, enabling growth recovery. In contrast to wild-type plants, plants, which are defective in damage-induced programmed cell death, maintain the cell identities and stereotypical structure of the stem cell niche after irradiation, but these cells fail to undergo cell division, terminating root growth. We propose DNA damage-induced programmed cell death is employed by plants as a developmental response, contrasting with its role as an anticarcinogenic response in animals. This role in plants may have evolved to restore the growth of embryos after the accumulation of DNA damage in seeds.

Citing Articles

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Waking up Sleeping Beauty: DNA damage activates dormant stem cell division by enhancing brassinosteroid signaling.

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Seed longevity and genome damage.

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Translational control of SOG1 expression in response to replication stress in Arabidopsis.

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References

Furukawa T, Curtis M, Tominey C, Duong Y, Wilcox B, Aggoune D . A shared DNA-damage-response pathway for induction of stem-cell death by UVB and by gamma irradiation. DNA Repair (Amst). 2010; 9(9):940-8. DOI: 10.1016/j.dnarep.2010.06.006. View

Sjogren C, Bolaris S, Larsen P . Aluminum-Dependent Terminal Differentiation of the Arabidopsis Root Tip Is Mediated through an ATR-, ALT2-, and SOG1-Regulated Transcriptional Response. Plant Cell. 2015; 27(9):2501-15. PMC: 4815104. DOI: 10.1105/tpc.15.00172. View

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

Ottenschlager I, Wolff P, Wolverton C, Bhalerao R, Sandberg G, Ishikawa H . Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A. 2003; 100(5):2987-91. PMC: 151453. DOI: 10.1073/pnas.0437936100. View

Ravi M, Marimuthu M, Tan E, Maheshwari S, Henry I, Marin-Rodriguez B . A haploid genetics toolbox for Arabidopsis thaliana. Nat Commun. 2014; 5:5334. DOI: 10.1038/ncomms6334. View

Curtis M, Hays J . Tolerance of dividing cells to replication stress in UVB-irradiated Arabidopsis roots: requirements for DNA translesion polymerases eta and zeta. DNA Repair (Amst). 2007; 6(9):1341-58. DOI: 10.1016/j.dnarep.2007.03.004. View

Hu Z, Cools T, De Veylder L . Mechanisms Used by Plants to Cope with DNA Damage. Annu Rev Plant Biol. 2015; 67:439-62. DOI: 10.1146/annurev-arplant-043015-111902. View

Menges M, Hennig L, Gruissem W, Murray J . Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol. 2004; 53(4):423-42. DOI: 10.1023/B:PLAN.0000019059.56489.ca. View

Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, Kondou Y . Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci U S A. 2011; 108(24):10004-9. PMC: 3116379. DOI: 10.1073/pnas.1103584108. View

10.

Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J . The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005; 433(7021):39-44. DOI: 10.1038/nature03184. View

11.

Hong J, Savina M, Du J, Devendran A, Ramakanth K, Tian X . A Sacrifice-for-Survival Mechanism Protects Root Stem Cell Niche from Chilling Stress. Cell. 2017; 170(1):102-113.e14. DOI: 10.1016/j.cell.2017.06.002. View

12.

Heyman J, Cools T, Vandenbussche F, Heyndrickx K, Van Leene J, Vercauteren I . ERF115 controls root quiescent center cell division and stem cell replenishment. Science. 2013; 342(6160):860-3. DOI: 10.1126/science.1240667. View

13.

Roitinger E, Hofer M, Kocher T, Pichler P, Novatchkova M, Yang J . 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. 2015; 14(3):556-71. PMC: 4349977. DOI: 10.1074/mcp.M114.040352. View

14.

Tsai H, Missirian V, Ngo K, Tran R, Chan S, Sundaresan V . Production of a high-efficiency TILLING population through polyploidization. Plant Physiol. 2013; 161(4):1604-14. PMC: 3613442. DOI: 10.1104/pp.112.213256. View

15.

Yoshiyama K, Conklin P, Huefner N, Britt A . Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc Natl Acad Sci U S A. 2009; 106(31):12843-8. PMC: 2722309. DOI: 10.1073/pnas.0810304106. View

16.

Einset J, Collins A . DNA repair after X-irradiation: lessons from plants. Mutagenesis. 2014; 30(1):45-50. DOI: 10.1093/mutage/geu054. View

17.

Huefner N, Yoshiyama K, Friesner J, Conklin P, Britt A . Genomic stability in response to high versus low linear energy transfer radiation in Arabidopsis thaliana. Front Plant Sci. 2014; 5:206. PMC: 4033213. DOI: 10.3389/fpls.2014.00206. View

18.

Yoshiyama K, Kobayashi J, Ogita N, Ueda M, Kimura S, Maki H . ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis. EMBO Rep. 2013; 14(9):817-22. PMC: 3790055. DOI: 10.1038/embor.2013.112. View

19.

Waterworth W, Footitt S, Bray C, Finch-Savage W, West C . DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds. Proc Natl Acad Sci U S A. 2016; 113(34):9647-52. PMC: 5003248. DOI: 10.1073/pnas.1608829113. View

20.

Sanchez Y, Bachant J, Wang H, Hu F, Liu D, Tetzlaff M . Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science. 1999; 286(5442):1166-71. DOI: 10.1126/science.286.5442.1166. View