Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis

Proc Natl Acad Sci U S A. 2011 Jun 14;108(24):10004-9. doi: 10.1073/pnas.1103584108. Epub 2011 May 25.

Abstract

Genome integrity is continuously threatened by external stresses and endogenous hazards such as DNA replication errors and reactive oxygen species. The DNA damage checkpoint in metazoans ensures genome integrity by delaying cell-cycle progression to repair damaged DNA or by inducing apoptosis. ATM and ATR (ataxia-telangiectasia-mutated and -Rad3-related) are sensor kinases that relay the damage signal to transducer kinases Chk1 and Chk2 and to downstream cell-cycle regulators. Plants also possess ATM and ATR orthologs but lack obvious counterparts of downstream regulators. Instead, the plant-specific transcription factor SOG1 (suppressor of gamma response 1) plays a central role in the transmission of signals from both ATM and ATR kinases. Here we show that in Arabidopsis, endoreduplication is induced by DNA double-strand breaks (DSBs), but not directly by DNA replication stress. When root or sepal cells, or undifferentiated suspension cells, were treated with DSB inducers, they displayed increased cell size and DNA ploidy. We found that the ATM-SOG1 and ATR-SOG1 pathways both transmit DSB-derived signals and that either one suffices for endocycle induction. These signaling pathways govern the expression of distinct sets of cell-cycle regulators, such as cyclin-dependent kinases and their suppressors. Our results demonstrate that Arabidopsis undergoes a programmed endoreduplicative response to DSBs, suggesting that plants have evolved a distinct strategy to sustain growth under genotoxic stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins
  • Bleomycin / toxicity
  • Cell Cycle Proteins / genetics
  • Cells, Cultured
  • Cisplatin / toxicity
  • DNA Breaks, Double-Stranded / drug effects*
  • DNA Breaks, Double-Stranded / radiation effects
  • DNA Damage*
  • DNA Replication / drug effects*
  • DNA Replication / radiation effects
  • DNA, Plant / genetics*
  • Gamma Rays
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental / drug effects
  • Gene Expression Regulation, Developmental / radiation effects
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / radiation effects
  • Methyl Methanesulfonate / toxicity
  • Mutagens / toxicity
  • Mutation
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Ploidies
  • Protein-Serine-Threonine Kinases / genetics
  • Signal Transduction / genetics
  • Transcription Factors / genetics
  • Ultraviolet Rays

Substances

  • ATM protein, Arabidopsis
  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • DNA, Plant
  • Mutagens
  • SOG1 protein, Arabidopsis
  • Transcription Factors
  • Bleomycin
  • Zeocin
  • Methyl Methanesulfonate
  • ATR protein, Arabidopsis
  • Ataxia Telangiectasia Mutated Proteins
  • Protein-Serine-Threonine Kinases
  • Cisplatin