Plants (Aug 2021)

<i>Arabidopsis thaliana</i> Response to Extracellular DNA: Self Versus Nonself Exposure

  • Maria Luisa Chiusano,
  • Guido Incerti,
  • Chiara Colantuono,
  • Pasquale Termolino,
  • Emanuela Palomba,
  • Francesco Monticolo,
  • Giovanna Benvenuto,
  • Alessandro Foscari,
  • Alfonso Esposito,
  • Lucia Marti,
  • Giulia de Lorenzo,
  • Isaac Vega-Muñoz,
  • Martin Heil,
  • Fabrizio Carteni,
  • Giuliano Bonanomi,
  • Stefano Mazzoleni

DOI
https://doi.org/10.3390/plants10081744
Journal volume & issue
Vol. 10, no. 8
p. 1744

Abstract

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The inhibitory effect of extracellular DNA (exDNA) on the growth of conspecific individuals was demonstrated in different kingdoms. In plants, the inhibition has been observed on root growth and seed germination, demonstrating its role in plant–soil negative feedback. Several hypotheses have been proposed to explain the early response to exDNA and the inhibitory effect of conspecific exDNA. We here contribute with a whole-plant transcriptome profiling in the model species Arabidopsis thaliana exposed to extracellular self- (conspecific) and nonself- (heterologous) DNA. The results highlight that cells distinguish self- from nonself-DNA. Moreover, confocal microscopy analyses reveal that nonself-DNA enters root tissues and cells, while self-DNA remains outside. Specifically, exposure to self-DNA limits cell permeability, affecting chloroplast functioning and reactive oxygen species (ROS) production, eventually causing cell cycle arrest, consistently with macroscopic observations of root apex necrosis, increased root hair density and leaf chlorosis. In contrast, nonself-DNA enters the cells triggering the activation of a hypersensitive response and evolving into systemic acquired resistance. Complex and different cascades of events emerge from exposure to extracellular self- or nonself-DNA and are discussed in the context of Damage- and Pathogen-Associated Molecular Patterns (DAMP and PAMP, respectively) responses.

Keywords