The bHLH Transcription Factor HBI1 Mediates the Trade-Off between Growth and Pathogen-Associated Molecular Pattern–Triggered Immunity in<i>Arabidopsis</i>

Fan, Min; Bai, Ming-Yi; Kim, Jung Gun; Wang, Tina; Oh, Eunkyoo; Chen, Lawrence R.; Park, Chan Ho; Son, Seung Hyun; Kim, Seong Ki; Mudgett, Mary Beth; Wang, Wenfei

doi:10.1105/tpc.113.121111

Cited by 198 publications

(180 citation statements)

References 70 publications

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“…Mitochondria dysfunction interferes with 9-LOX and BR signaling (Bekh-Ochir et al, 2013;Vellosillo et al, 2013) and might unbalance ROS production, a key process in the control of plant development and plant defense. Recent studies indicate BR pathway involvement in plant immunity and its role in balancing defense versus growth (Belkhadir et al, 2014;Fan et al, 2014). Our results show the sequential participation of the 9-LOX and BR pathways in triggering cell wallbased plant defense; in response to pathogen inoculation, oxylipins might function as ROS signals to activate the BR pathway and contribute to cell wall reinforcement and plant defense.…”

Section: Discussionmentioning

confidence: 77%

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

et al. 2015

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The oxylipins, a large family of oxygenated lipid derivatives, regulate plant development and immunity. Two members of the 9-lipoxygenase (9-LOX) oxylipin pathway, 9-hydroxyoctadecatrienoic acid and 9-ketooctadecatrienoic acid, control root development and plant defense. Studies in Arabidopsis (Arabidopsis thaliana) using a series of 9-hydroxyoctadecatrienoic acidand 9-ketooctadecatrienoic acid-insensitive nonresponding to oxylipins (noxy) mutants showed the importance of the cell wall as a 9-LOX-induced defense component and the participation of NOXY proteins in signaling cell wall damage. Here, we examined 9-LOX signaling using the mutants lox1lox5, which lacks 9-LOX activity, and noxy2-2, which shows oxylipin insensitivity and mitochondrial dysfunction. Mutants in brassinosteroids (BRs), a class of plant hormones necessary for normal plant growth and the control of cell wall integrity, were also analyzed. Several lines of evidence indicated that 9-LOX-derived oxylipins induce BR synthesis and signaling to activate cell wall-based responses such as callose deposition and that constitutive activation of BR signaling in bri1-EMS-suppressor 1-D (bes1-D) plants enhances this response. We found that constitutive BR signaling in bes1-D and brassinolide-resistant 1-1D (bzr1-1D) mutants conferred resistance to Pseudomonas syringae. bes1-D and bzr1-1D showed increased resistance to Golovinomyces cichoracearum, an obligate biotrophic fungus that penetrates the cell wall for successful infection, whereas susceptibility was enhanced in lox1lox5 and noxy2-2. Our results indicate a sequential action of 9-LOX and BR signaling in activating cell wall-based defense, and this response prevents pathogen infection. These results show interaction between the 9-LOX and BR pathways and help to clarify their role in modulating plant defense.

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Section: Discussionmentioning

confidence: 77%

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

et al. 2015

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“…Due to the sessile lifestyle of plants and the limitation of available energy, plants have evolved an elaborate regulatory network to effect a tradeoff between growth and immune responses to ensure plant survival under fluctuating environments (Kazan and Manners, 2009;Fan et al, 2014). V. dahliae is notorious for its infection strategies and great genetic plasticity, and it causes significant economic losses for a broad range of crops, such as cotton, strawberry (Fragaria 3 ananassa), oilseed rape (Brassica napus), tomato (Solanum lycopersicum), and Figure 6.…”

Section: Discussionmentioning

confidence: 99%

Cotton WRKY1 Mediates the Plant Defense-to-Development Transition during Infection of Cotton byVerticillium dahliaeby ActivatingJASMONATE ZIM-DOMAIN1Expression

Luo

et al. 2014

Plant Physiology

138

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Plants have evolved an elaborate signaling network to ensure an appropriate level of immune response to meet the differing demands of developmental processes. Previous research has demonstrated that DELLA proteins physically interact with JASMONATE ZIM-DOMAIN1 (JAZ1) and dynamically regulate the interaction of the gibberellin (GA) and jasmonate (JA) signaling pathways. However, whether and how the JAZ1-DELLA regulatory node is regulated at the transcriptional level in plants under normal growth conditions or during pathogen infection is not known. Here, we demonstrate multiple functions of cotton (Gossypium barbadense) GbWRKY1 in the plant defense response and during development. Although GbWRKY1 expression is induced rapidly by methyl jasmonate and infection by Verticillium dahliae, our results show that GbWRKY1 is a negative regulator of the JA-mediated defense response and plant resistance to the pathogens Botrytis cinerea and V. dahliae. Under normal growth conditions, GbWRKY1-overexpressing lines displayed GA-associated phenotypes, including organ elongation and early flowering, coupled with the down-regulation of the putative targets of DELLA. We show that the GA-related phenotypes of GbWRKY1-overexpressing plants depend on the constitutive expression of Gossypium hirsutum GhJAZ1. We also show that GhJAZ1 can be transactivated by GbWRKY1 through TGAC core sequences, and the adjacent sequences of this binding site are essential for binding specificity and affinity to GbWRKY1, as revealed by dual-luciferase reporter assays and electrophoretic mobility shift assays. In summary, our data suggest that GbWRKY1 is a critical regulator mediating the plant defense-to-development transition during V. dahliae infection by activating JAZ1 expression.

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“…RIN4 is a known target of multiple effectors (Jones and Dangl, 2006). HBI1 is a basic helix-loop-helix TF that mediates the tradeoff between plant growth and the immune response (Fan et al, 2014). Functional enrichment analysis indicated that development and defense are the most prominent themes in this subnetwork.…”

Section: Identification Of a Shared Subnetwork Between Pti And Etimentioning

confidence: 99%

Revealing Shared and Distinct Gene Network Organization in Arabidopsis Immune Responses by Integrative Analysis

et al. 2015

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Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) are two main plant immune responses to counter pathogen invasion. Genome-wide gene network organizing principles leading to quantitative differences between PTI and ETI have remained elusive. We combined an advanced machine learning method and modular network analysis to systematically characterize the organizing principles of Arabidopsis (Arabidopsis thaliana) PTI and ETI at three network resolutions. At the single network node/ edge level, we ranked genes and gene interactions based on their ability to distinguish immune response from normal growth and successfully identified many immune-related genes associated with PTI and ETI. Topological analysis revealed that the top-ranked gene interactions tend to link network modules. At the subnetwork level, we identified a subnetwork shared by PTI and ETI encompassing 1,159 genes and 1,289 interactions. This subnetwork is enriched in interactions linking network modules and is also a hotspot of attack by pathogen effectors. The subnetwork likely represents a core component in the coordination of multiple biological processes to favor defense over development. Finally, we constructed modular network models for PTI and ETI to explain the quantitative differences in the global network architecture. Our results indicate that the defense modules in ETI are organized into relatively independent structures, explaining the robustness of ETI to genetic mutations and effector attacks. Taken together, the multiscale comparisons of PTI and ETI provide a systems biology perspective on plant immunity and emphasize coordination among network modules to establish a robust immune response.

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The bHLH Transcription Factor HBI1 Mediates the Trade-Off between Growth and Pathogen-Associated Molecular Pattern–Triggered Immunity inArabidopsis

Cited by 198 publications

References 70 publications

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

9-Lipoxygenase-derived oxylipins activate brassinosteroid signaling to promote cell wall-based defense and limit pathogen infection

Cotton WRKY1 Mediates the Plant Defense-to-Development Transition during Infection of Cotton byVerticillium dahliaeby ActivatingJASMONATE ZIM-DOMAIN1Expression

Revealing Shared and Distinct Gene Network Organization in Arabidopsis Immune Responses by Integrative Analysis

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