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PLoS Genet. 2013;9(12):e1004015. doi: 10.1371/journal.pgen.1004015. Epub 2013 Dec 12.

Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana.

Author information

1
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany ; Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St. Paul, Minnesota, United States of America.
2
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
3
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St. Paul, Minnesota, United States of America.
4
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St. Paul, Minnesota, United States of America ; Institute for Innovation, Ajinomoto Co., Inc., 1-1, Suzuki-cho, Kawasaki-ku, Kawasaki, Japan.
5
Department of Biological Sciences, Chicago State University, Chicago, Illinois, United States of America.
6
National Institute for Basic Biology, Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Higashiyama, Myodaiji, Okazaki, Japan.

Abstract

Network robustness is a crucial property of the plant immune signaling network because pathogens are under a strong selection pressure to perturb plant network components to dampen plant immune responses. Nevertheless, modulation of network robustness is an area of network biology that has rarely been explored. While two modes of plant immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), extensively share signaling machinery, the network output is much more robust against perturbations during ETI than PTI, suggesting modulation of network robustness. Here, we report a molecular mechanism underlying the modulation of the network robustness in Arabidopsis thaliana. The salicylic acid (SA) signaling sector regulates a major portion of the plant immune response and is important in immunity against biotrophic and hemibiotrophic pathogens. In Arabidopsis, SA signaling was required for the proper regulation of the vast majority of SA-responsive genes during PTI. However, during ETI, regulation of most SA-responsive genes, including the canonical SA marker gene PR1, could be controlled by SA-independent mechanisms as well as by SA. The activation of the two immune-related MAPKs, MPK3 and MPK6, persisted for several hours during ETI but less than one hour during PTI. Sustained MAPK activation was sufficient to confer SA-independent regulation of most SA-responsive genes. Furthermore, the MPK3 and SA signaling sectors were compensatory to each other for inhibition of bacterial growth as well as for PR1 expression during ETI. These results indicate that the duration of the MAPK activation is a critical determinant for modulation of robustness of the immune signaling network. Our findings with the plant immune signaling network imply that the robustness level of a biological network can be modulated by the activities of network components.

PMID:
24348271
PMCID:
PMC3861249
DOI:
10.1371/journal.pgen.1004015
[Indexed for MEDLINE]
Free PMC Article

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