Research Article: Microbial Pathogens Trigger Host DNA Double-Strand Breaks Whose Abundance Is Reduced by Plant Defense Responses

Date Published: April 3, 2014

Publisher: Public Library of Science

Author(s): Junqi Song, Andrew F. Bent, Shengyang He.


Immune responses and DNA damage repair are two fundamental processes that have been characterized extensively, but the links between them remain largely unknown. We report that multiple bacterial, fungal and oomycete plant pathogen species induce double-strand breaks (DSBs) in host plant DNA. DNA damage detected by histone γ-H2AX abundance or DNA comet assays arose hours before the disease-associated necrosis caused by virulent Pseudomonas syringae pv. tomato. Necrosis-inducing paraquat did not cause detectable DSBs at similar stages after application. Non-pathogenic E. coli and Pseudomonas fluorescens bacteria also did not induce DSBs. Elevation of reactive oxygen species (ROS) is common during plant immune responses, ROS are known DNA damaging agents, and the infection-induced host ROS burst has been implicated as a cause of host DNA damage in animal studies. However, we found that DSB formation in Arabidopsis in response to P. syringae infection still occurs in the absence of the infection-associated oxidative burst mediated by AtrbohD and AtrbohF. Plant MAMP receptor stimulation or application of defense-activating salicylic acid or jasmonic acid failed to induce a detectable level of DSBs in the absence of introduced pathogens, further suggesting that pathogen activities beyond host defense activation cause infection-induced DNA damage. The abundance of infection-induced DSBs was reduced by salicylic acid and NPR1-mediated defenses, and by certain R gene-mediated defenses. Infection-induced formation of γ-H2AX still occurred in Arabidopsis atr/atm double mutants, suggesting the presence of an alternative mediator of pathogen-induced H2AX phosphorylation. In summary, pathogenic microorganisms can induce plant DNA damage. Plant defense mechanisms help to suppress rather than promote this damage, thereby contributing to the maintenance of genome integrity in somatic tissues.

Partial Text

Organisms continuously encounter many types of DNA damage and have evolved elegant mechanisms to maintain their genomic integrity [1], [2]. DNA damage can be induced by a variety of exogenous stresses such as ultraviolet light or genotoxic chemicals, and by endogenous insults such as reactive oxygen species and DNA replication errors [1]–[3]. DNA double-strand breaks (DSBs) can trigger cell cycle arrest and programmed cell death, and are among the most serious types of DNA damage. Surveillance for DSBs and signaling in response to DSBs are therefore critical for cells to orchestrate DNA repair pathways not only in the germ line but also in somatic tissues, to sustain genome stability and survival of the organism [1], [2].

The present study discovered that host DNA damage is induced, both in the model organism Arabidopsis thaliana and in tomato and potato crop plants, in response to plant pathogens with diverse life styles including a hemibiotrophic bacterial species, an oomycete and a necrotrophic fungus. Similar or reduced levels of DNA DSBs were induced during incompatible interactions when compared with compatible interactions. Plant defense mediators such as ROS, jasmonic acid and MAMP receptors did not on their own increase DSBs, and SA-mediated defenses reduced rather than elevated pathogen-induced DNA damage. These findings provide a new type of evidence of links between the plant immune and DNA damage responses. Prevention and repair of DNA damage is needed, to a greater extent than was previously understood, as an element of the plant defense response.




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