Integration of stress-related and reactive oxygen species-mediated signals by Topoisomerase VI in Arabidopsis thaliana

Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):16360-5. doi: 10.1073/pnas.1202041109. Epub 2012 Sep 17.


Environmental stress often leads to an increased production of reactive oxygen species that are involved in plastid-to-nucleus retrograde signaling. Soon after the release of singlet oxygen ((1)O(2)) in chloroplasts of the flu mutant of Arabidopsis, reprogramming of nuclear gene expression reveals a rapid transfer of signals from the plastid to the nucleus. We have identified extraplastidic signaling constituents involved in (1)O(2)-initiated plastid-to-nucleus signaling and nuclear gene activation after mutagenizing a flu line expressing the luciferase reporter gene under the control of the promoter of a (1)O(2)-responsive AAA-ATPase gene (At3g28580) and isolating second-site mutations that lead to a constitutive up-regulation of the reporter gene or abrogate its (1)O(2)-dependent up-regulation. One of these mutants, caa39, turned out to be a weak mutant allele of the Topoisomerase VI (Topo VI) A-subunit gene with a single amino acid substitution. Transcript profile analysis of flu and flu caa39 mutants revealed that Topo VI is necessary for the full activation of AAA-ATPase and a set of (1)O(2)-responsive transcripts in response to (1)O(2). Topo VI binds to the promoter of the AAA-ATPase and other (1)O(2)-responsive genes, and hence could directly regulate their expression. Under photoinhibitory stress conditions, which enhance the production of (1)O(2) and H(2)O(2), Topo VI regulates (1)O(2)-responsive and H(2)O(2)-responsive genes in a distinct manner. These results suggest that Topo VI acts as an integrator of multiple signals generated by reactive oxygen species formed in plants under adverse environmental conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology*
  • Arabidopsis Proteins / genetics
  • Archaeal Proteins / metabolism*
  • Cell Nucleus / metabolism
  • Chromatin Immunoprecipitation
  • DNA Topoisomerases, Type II / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology*
  • Luciferases
  • Microarray Analysis
  • Mutation / genetics
  • Plastids / metabolism
  • Reactive Oxygen Species / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Singlet Oxygen / metabolism
  • Stress, Physiological / physiology*


  • Arabidopsis Proteins
  • Archaeal Proteins
  • FLU protein, Arabidopsis
  • Reactive Oxygen Species
  • Singlet Oxygen
  • Luciferases
  • DNA topoisomerase VI
  • DNA Topoisomerases, Type II