The growth–defense pivot: crisis management in plants mediated by LRR-RK surface receptors

Belkhadir, Youssef; Yang, Li; Hetzel, Jonathan; Dangl, Jeffery L.; Chory, Joanne

doi:10.1016/j.tibs.2014.06.006

Cited by 132 publications

(122 citation statements)

References 105 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: 56%

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: 56%

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

et al. 2015

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“…Effective plant immunity requires the efficient perception of potentially pathogenic microbial-associated molecular patterns (MAMPs) by a range of host-encoded extracellular pattern recognition receptors (PRRs) (Belkhadir et al, 2014;Böhm et al, 2014;Macho and Zipfel, 2014;Zipfel, 2014). These stimuli are translated into the rapid transcriptional activation of a network of MAMP-triggered immunity (MTI) responses (Buscaill and Rivas, 2014).…”

Section: Introductionmentioning

confidence: 99%

Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000

et al. 2015

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Transcriptional reprogramming is integral to effective plant defense. Pathogen effectors act transcriptionally and posttranscriptionally to suppress defense responses. A major challenge to understanding disease and defense responses is discriminating between transcriptional reprogramming associated with microbial-associated molecular pattern (MAMP)-triggered immunity (MTI) and that orchestrated by effectors. A high-resolution time course of genome-wide expression changes following challenge with Pseudomonas syringae pv tomato DC3000 and the nonpathogenic mutant strain DC3000hrpA-allowed us to establish causal links between the activities of pathogen effectors and suppression of MTI and infer with high confidence a range of processes specifically targeted by effectors. Analysis of this information-rich data set with a range of computational tools provided insights into the earliest transcriptional events triggered by effector delivery, regulatory mechanisms recruited, and biological processes targeted. We show that the majority of genes contributing to disease or defense are induced within 6 h postinfection, significantly before pathogen multiplication. Suppression of chloroplast-associated genes is a rapid MAMP-triggered defense response, and suppression of genes involved in chromatin assembly and induction of ubiquitin-related genes coincide with pathogen-induced abscisic acid accumulation. Specific combinations of promoter motifs are engaged in fine-tuning the MTI response and active transcriptional suppression at specific promoter configurations by P. syringae.

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“…BRs are perceived at the cell surface by Brassinosteroid Insensitive 1 (BRI1), a leucine-rich repeat (LRR)-receptor kinase, which is the central receptor controlling root growth, and with a broad expression pattern in the root meristem. Activated BRI1 phosphorylates its negative regulator Brassinsosteroid Kinase Inhibitor 1 (BKI1) (4,5), which enables BRI1 to form a complex with its coreceptor BRI1-Associated Kinase 1 (BAK1) (6,7). The activated receptor triggers transmission of the BR signal to the nucleus, after various regulatory steps, including inhibition of GSK3-like kinase Brassinosteroid Insensitive 2 (BIN2), the key inhibitor of the signaling cascade.…”

mentioning

confidence: 99%

Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation

Vragović

Sela

Friedlander-Shani

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

118

164

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The mechanisms ensuring balanced growth remain a critical question in developmental biology. In plants, this balance relies on spatiotemporal integration of hormonal signaling pathways, but the understanding of the precise contribution of each hormone is just beginning to take form. Brassinosteroid (BR) hormone is shown here to have opposing effects on root meristem size, depending on its site of action. BR is demonstrated to both delay and promote onset of stem cell daughter differentiation, when acting in the outer tissue of the root meristem, the epidermis, and the innermost tissue, the stele, respectively. To understand the molecular basis of this phenomenon, a comprehensive spatiotemporal translatome mapping of Arabidopsis roots was performed. Analyses of wild type and mutants featuring different distributions of BR revealed autonomous, tissuespecific gene responses to BR, implying its contrasting tissue-dependent impact on growth. BR-induced genes were primarily detected in epidermal cells of the basal meristem zone and were enriched by auxinrelated genes. In contrast, repressed BR genes prevailed in the stele of the apical meristem zone. Furthermore, auxin was found to mediate the growth-promoting impact of BR signaling originating in the epidermis, whereas BR signaling in the stele buffered this effect. We propose that context-specific BR activity and responses are oppositely interpreted at the organ level, ensuring coherent growth.

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The growth–defense pivot: crisis management in plants mediated by LRR-RK surface receptors

Cited by 132 publications

References 105 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

Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000

Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation

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