Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana
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 ofmore »
- Authors:
-
- Max Planck Institute for Plant Breeding Research, Cologne (Germany); University of Minnesota, Minneapolis, MN (United States)
- Max Planck Institute for Plant Breeding Research, Cologne (Germany)
- University of Minnesota, Minneapolis, MN (United States)
- University of Minnesota, Minneapolis, MN (United States); Institute for Innovation, Ajinomoto Co., Inc., Kawasaki (Japan)
- Chicago State University, IL (United States)
- National Institutes of Natural Sciences, Okazaki (Japan)
- Publication Date:
- Research Org.:
- Univ. of Minnesota, Minneapolis, MN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); Max Planck Society; National Science Foundation (NSF); Japan Society for the Promotion of Science (JSPS)
- OSTI Identifier:
- 1904660
- Grant/Contract Number:
- FG02-05ER15670; MCB-0918908; IOS-1121425
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 12; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; MAPK signaling cascades; gene regulation; leaves; Arabidopsis thaliana; signaling networks; gene expression; plant disease resistance; seedings
Citation Formats
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, and Katagiri, Fumiaki. Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana. United States: N. p., 2013.
Web. doi:10.1371/journal.pgen.1004015.
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, & Katagiri, Fumiaki. Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana. United States. https://doi.org/10.1371/journal.pgen.1004015
Tsuda, Kenichi, Mine, Akira, Bethke, Gerit, Igarashi, Daisuke, Botanga, Christopher J., Tsuda, Yayoi, Glazebrook, Jane, Sato, Masanao, and Katagiri, Fumiaki. Thu .
"Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana". United States. https://doi.org/10.1371/journal.pgen.1004015. https://www.osti.gov/servlets/purl/1904660.
@article{osti_1904660,
title = {Dual Regulation of Gene Expression Mediated by Extended MAPK Activation and Salicylic Acid Contributes to Robust Innate Immunity in Arabidopsis thaliana},
author = {Tsuda, Kenichi and Mine, Akira and Bethke, Gerit and Igarashi, Daisuke and Botanga, Christopher J. and Tsuda, Yayoi and Glazebrook, Jane and Sato, Masanao and Katagiri, Fumiaki},
abstractNote = {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.},
doi = {10.1371/journal.pgen.1004015},
journal = {PLoS Genetics},
number = 12,
volume = 9,
place = {United States},
year = {Thu Dec 12 00:00:00 EST 2013},
month = {Thu Dec 12 00:00:00 EST 2013}
}
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