A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity

Humphry, Matt; Bednarek, Paweł; Kemmerling, Birgit; Koh, Sung-Cheol; Stein, Mónica; Göbel, Ulrike; Stüber, Kurt; Piślewska‐Bednarek, Mariola; Loraine, Ann E.; Schulze‐Lefert, Paul; Somerville, Shauna; Panstruga, Ralph

doi:10.1073/pnas.1003619107

Cited by 98 publications

(93 citation statements)

References 33 publications

(48 reference statements)

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“…S2). An evolutionarily conserved regulon was previously identified in barley and Arabidopsis upon comparative coexpression analysis of genetically defined immune components that restrict the growth of fungal pathogens, including powdery mildews (16). Strikingly, the functionally validated antifungal regulon also showed sustained transcript accumulation at 18 hpi in our data set (Fig.…”

Section: Resultsmentioning

confidence: 50%

Conservation of NLR-triggered immunity across plant lineages

Maekawa

Kracher

Vernaldi

et al. 2012

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

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The nucleotide-binding domain and leucine-rich repeat (NLR) family of plant receptors detects pathogen-derived molecules, designated effectors, inside host cells and mediates innate immune responses to pathogenic invaders. Genetic evidence revealed species-specific coevolution of many NLRs with effectors from host-adapted pathogens, suggesting that the specificity of these NLRs is restricted to the host or closely related plant species. However, we report that an NLR immune receptor (MLA1) from monocotyledonous barley is fully functional in partially immunocompromised dicotyledonous Arabidopsis thaliana against the barley powdery mildew fungus, Blumeria graminis f. sp. hordei. This implies ∼200 million years of evolutionary conservation of the underlying immune mechanism. A time-course RNA-seq analysis in transgenic Arabidopsis lines detected sustained expression of a large MLA1-dependent gene cluster. This cluster is greatly enriched in genes known to respond to the fungal cell wallderived microbe-associated molecular pattern chitin. The MLA1-dependent sustained transcript accumulation could define a conserved function of the nuclear pool of MLA1 detected in barley and Arabidopsis. We also found that MLA1-triggered immunity was fully retained in mutant plants that are simultaneously depleted of ethylene, jasmonic acid, and salicylic acid signaling. This points to the existence of an evolutionarily conserved and phytohormone-independent MLA1-mediated resistance mechanism. This also suggests a conserved mechanism for internalization of B. graminis f. sp. hordei effectors into host cells of flowering plants. Furthermore, the deduced connectivity of the NLR to multiple branches of immune signaling pathways likely confers increased robustness against pathogen effector-mediated interception of host immune signaling and could have contributed to the evolutionary preservation of the immune mechanism.innate immunity | defense phytohormone T he nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins in plants and animals mediate pathogensensing. Unlike animal NLRs that detect mostly conserved microbial molecules, plant-encoded NLRs typically recognize the presence of isolate-specific pathogen effectors (1). Most plant NLRs are modular, containing coiled-coil (CC) or TOLL/IL-1 receptor domains at the N terminus, a central nucleotide-binding domain, and C-terminal leucine-rich repeats. Plant NLRs are often polymorphic between individual plants of a host population, and the sum of genes encoding NLRs in a host population defines the repertoire available for the detection of structure or action of polymorphic pathogen effectors (1).Interfamily transfer of NLR function was shown by coexpression of an NLR, its cognate effector and the effector target (e.g., Arabidopsis RPS5, Pseudomonas syringae AvrPphB, and Arabidopsis PBS1; reviewed in ref.2). However, these data are based on transient gene expression and use host cell death as proxy for NLR activity even though cell death has been uncoupled from NLRmedia...

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Section: Resultsmentioning

confidence: 50%

Conservation of NLR-triggered immunity across plant lineages

Maekawa

Kracher

Vernaldi

et al. 2012

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

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“…Although it is plausible to assume that conserved expression contexts are the output of ancestral regulatory interactions that have been conserved in extant species (Humphry et al, 2010), the absence of largescale TF-target data makes it difficult to construct genome-wide regulatory networks in plants and to The categories "cons," "div," and "non" indicate conserved, diverged, and not significant, respectively. directly study their evolution.…”

Section: Discussionmentioning

confidence: 99%

Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice

2011

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Microarray experiments have yielded massive amounts of expression information measured under various conditions for the model species Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Expression compendia grouping multiple experiments make it possible to define correlated gene expression patterns within one species and to study how expression has evolved between species. We developed a robust framework to measure expression context conservation (ECC) and found, by analyzing 4,630 pairs of orthologous Arabidopsis and rice genes, that 77% showed conserved coexpression. Examples of nonconserved ECC categories suggested a link between regulatory evolution and environmental adaptations and included genes involved in signal transduction, response to different abiotic stresses, and hormone stimuli. To identify genomic features that influence expression evolution, we analyzed the relationship between ECC, tissue specificity, and protein evolution. Tissue-specific genes showed higher expression conservation compared with broadly expressed genes but were fast evolving at the protein level. No significant correlation was found between protein and expression evolution, implying that both modes of gene evolution are not strongly coupled in plants. By integration of cis-regulatory elements, many ECC conserved genes were significantly enriched for shared DNA motifs, hinting at the conservation of ancestral regulatory interactions in both model species. Surprisingly, for several tissue-specific genes, patterns of concerted network evolution were observed, unveiling conserved coexpression in the absence of conservation of tissue specificity. These findings demonstrate that orthologs inferred through sequence similarity in many cases do not share similar biological functions and highlight the importance of incorporating expression information when comparing genes across species.

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“…S7). Because this step in fungal pathogenesis requires entry of fungal germlings into host cells (30,31), this assigns to SYP42 and SYP43 a function in secretion-dependent disease resistance responses.…”

Section: Syp4 Proteins Are Required To Maintain the Morphology Of Thementioning

confidence: 99%

Qa-SNAREs localized to the trans -Golgi network regulate multiple transport pathways and extracellular disease resistance in plants

Uemura

Kim

Saito

et al. 2012

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

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156

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In all eukaryotic cells, a membrane-trafficking system connects the post-Golgi organelles, such as the trans-Golgi network (TGN), endosomes, vacuoles, and the plasma membrane. This complex network plays critical roles in several higher-order functions in multicellular organisms. The TGN, one of the important organelles for protein transport in the post-Golgi network, functions as a sorting station, where cargo proteins are directed to the appropriate post-Golgi compartments. Unlike its roles in animal and yeast cells, the TGN has also been reported to function like early endosomal compartments in plant cells. However, the physiological roles of the TGN functions in plants are not understood. Here, we report a study of the SYP4 group (SYP41, SYP42, and SYP43), which represents the plant orthologs of the Tlg2/syntaxin16 Qa-SNARE (soluble N-ethylmaleimide sensitive factor attachment protein receptor) that localizes on the TGN in yeast and animal cells. The SYP4 group regulates the secretory and vacuolar transport pathways in the post-Golgi network and maintains the morphology of the Golgi apparatus and TGN. Consistent with a secretory role, SYP4 proteins are required for extracellular resistance responses to a fungal pathogen. We also reveal a plant cell-specific higher-order role of the SYP4 group in the protection of chloroplasts from salicylic acid-dependent biotic stress.Arabidopsis | membrane traffic | membrane fusion I n eukaryotic cells, membrane fusion is an essential process in protein secretion and endocytosis (1, 2). Selective membrane fusion occurs with the concerted functions of several molecules, including SNAREs (soluble N-ethylmaleimide sensitive factor attachment protein receptors), Rab GTPases, tethering factors, and Sec1p/Munc18 (SM) proteins. SNAREs are membrane-anchored proteins that contain α-helical heptad repeats and a characteristic central amino acid within the SNARE motif. The SNARE complex comprises four SNAREs, including three with a central glutamine residue in SNARE motif (Q-SNAREs: Qa, Qb, and Qc) and one with a central arginine (R-SNARE) in SNARE motif. The Q-SNAREs reside on the target membrane, and the R-SNARE resides on the transport vesicle. This complex first forms a bridge between the target organelle membrane and the vesicle, and then compresses to bring the two membranes close enough to mediate specific membrane fusion. After fusion is complete, the SNARE complex is dissociated by a NSF (N-ethylmaleimide-sensitive factor), and the SNAREs are recycled. To execute the correct membrane fusion, SNAREs must be localized on the membrane of specific organelles or transport vesicles. QaSNAREs also serve as organelle markers (3-5), by virtue of their specific localization on the membrane of target organelles.The TGN was first defined as a special organelle on the transside of the Golgi stack that is responsible for protein sorting to the plasma membrane or lysosomes (6). The TGN contains multiple sorting domains and functions as the compartment of cargo sorting. In addition, the TGN ...

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A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity

Cited by 98 publications

References 33 publications

Conservation of NLR-triggered immunity across plant lineages

Conservation of NLR-triggered immunity across plant lineages

Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice

Qa-SNAREs localized to the trans -Golgi network regulate multiple transport pathways and extracellular disease resistance in plants

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