scholarly journals Subfamily-Specific Specialization of RGH1/MLA Immune Receptors in Wild Barley

2019 ◽  
Vol 32 (1) ◽  
pp. 107-119 ◽  
Author(s):  
Takaki Maekawa ◽  
Barbara Kracher ◽  
Isabel M. L. Saur ◽  
Makoto Yoshikawa-Maekawa ◽  
Ronny Kellner ◽  
...  
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Geographic Origin ◽  
Coiled Coil ◽  
Hordeum Spontaneum ◽  
R Gene ◽  
Powdery Mildew Fungus ◽  
Signaling Domain ◽  
Pathogen Populations ◽  
Signaling Domains

The barley disease resistance (R) gene locus mildew locus A (Mla) provides isolate-specific resistance against the powdery mildew fungus Blumeria graminis hordei and has been introgressed into modern cultivars from diverse germplasms, including the wild relative Hordeum spontaneum. Known Mla disease resistance specificities to B. graminis hordei appear to encode allelic variants of the R gene homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. Here, we sequenced and assembled the transcriptomes of 50 H. spontaneum accessions representing nine populations distributed throughout the Fertile Crescent. The assembled Mla transcripts exhibited rich sequence diversity, linked neither to geographic origin nor population structure, and could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil (CC) signaling domains that are both capable of eliciting cell death. The presence of positively selected sites located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both CC signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the population. Unexpectedly, known MLA receptor variants that confer B. graminis hordei resistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially as adaptation to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor. [Formula: see text] Copyright © 2018 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

scholarly journals Population and Evolutionary Genetics Subfamily-specific functionalization of diversified immune receptors in wild barley

2018 ◽  
Author(s):  
Takaki Maekawa ◽  
Barbara Kracher ◽  
Isabel M. L. Saur ◽  
Makoto Yoshikawa-Maekawa ◽  
Ronny Kellner ◽  
...  
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Wild Barley ◽  
Geographic Origin ◽  
Coiled Coil ◽  
Evolutionary Genetics ◽  
Host Population ◽  
Powdery Mildew Fungus ◽  
Immune Receptors ◽  
Signaling Domains

AbstractGene-for-gene immunity between plants and host-adapted pathogens is often linked to population-level diversification of immune receptors encoded by disease resistance (R) genes. The complex barley (Hordeum vulgare L.) R gene locus Mildew Locus A (Mla) provides isolate-specific resistance against the powdery mildew fungus Blumeria graminis f. sp. hordei (Bgh) and has been introgressed into modern barley cultivars from diverse germplasms, including the wild relative H. spontaneum. Known Mla disease resistance specificities to Bgh appear to encode allelic variants of the R Gene Homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. To gain insights into Mla diversity in wild barley populations, we here sequenced and assembled the transcriptomes of 50 accessions of H. spontaneum representing nine populations distributed throughout the Fertile Crescent. The assembled Mla transcripts exhibited rich sequence diversity, which is linked neither to geographic origin nor population structure. Mla transcripts in the tested H. spontaneum accessions could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil signaling domains that are both capable of eliciting cell death. The presence of positively selected sites, located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both coiled-coil signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the host population. Unexpectedly, known MLA receptor variants that confer Bgh resistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor.

scholarly journals Induced proximity of a TIR signaling domain on a plant-mammalian NLR chimera activates defense in plants

2020 ◽  
Vol 117 (31) ◽  
pp. 18832-18839 ◽  
Author(s):  
Zane Duxbury ◽  
Shanshan Wang ◽  
Craig I. MacKenzie ◽  
Jeannette L. Tenthorey ◽  
Xiaoxiao Zhang ◽  
...  
Keyword(s):  
Plant Defense ◽  
Interleukin 1 ◽  
Coiled Coil ◽  
Leucine Rich Repeat ◽  
In Planta ◽  
Tir Domain ◽  
Signaling Mechanisms ◽  
Signaling Domain ◽  
Resistance Protein ◽  
Signaling Domains

Plant and animal intracellular nucleotide-binding, leucine-rich repeat (NLR) immune receptors detect pathogen-derived molecules and activate defense. Plant NLRs can be divided into several classes based upon their N-terminal signaling domains, including TIR (Toll-like, Interleukin-1 receptor, Resistance protein)- and CC (coiled-coil)-NLRs. Upon ligand detection, mammalian NAIP and NLRC4 NLRs oligomerize, forming an inflammasome that induces proximity of its N-terminal signaling domains. Recently, a plant CC-NLR was revealed to form an inflammasome-like hetero-oligomer. To further investigate plant NLR signaling mechanisms, we fused the N-terminal TIR domain of several plant NLRs to the N terminus of NLRC4. Inflammasome-dependent induced proximity of the TIR domain in planta initiated defense signaling. Thus, induced proximity of a plant TIR domain imposed by oligomerization of a mammalian inflammasome is sufficient to activate authentic plant defense. Ligand detection and inflammasome formation is maintained when the known components of the NLRC4 inflammasome is transferred across kingdoms, indicating that NLRC4 complex can robustly function without any additional mammalian proteins. Additionally, we found NADase activity of a plant TIR domain is necessary for plant defense activation, but NADase activity of a mammalian or a bacterial TIR is not sufficient to activate defense in plants.

scholarly journals The Chloroplastic Protein THF1 Interacts with the Coiled-Coil Domain of the Disease Resistance Protein N′ and Regulates Light-Dependent Cell Death

2016 ◽  
Vol 171 (1) ◽  
pp. 658-674 ◽  
Author(s):  
Louis-Philippe Hamel ◽  
Ken-Taro Sekine ◽  
Thérèse Wallon ◽  
Yuji Sugiwaka ◽  
Kappei Kobayashi ◽  
...  
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Coiled Coil ◽  
Coiled Coil Domain ◽  
Disease Resistance Protein ◽  
Dependent Cell ◽  
Resistance Protein

scholarly journals Induction of Xa10-like Genes in Rice Cultivar Nipponbare Confers Disease Resistance to Rice Bacterial Blight

2017 ◽  
Vol 30 (6) ◽  
pp. 466-477 ◽  
Author(s):  
Jun Wang ◽  
Dongsheng Tian ◽  
Keyu Gu ◽  
Xiaobei Yang ◽  
Lanlan Wang ◽  
...  
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Bacterial Blight ◽  
Rice Cultivar ◽  
R Gene ◽  
Transcription Activator ◽  
Knock Out ◽  
Tal Effector ◽  
Rice Bacterial Blight ◽  
Specific Disease

Bacterial blight of rice, caused by Xanthomonas oryzae pv. oryzae, is one of the most destructive bacterial diseases throughout the major rice-growing regions in the world. The rice disease resistance (R) gene Xa10 confers race-specific disease resistance to X. oryzae pv. oryzae strains that deliver the corresponding transcription activator-like (TAL) effector AvrXa10. Upon bacterial infection, AvrXa10 binds specifically to the effector binding element in the promoter of the R gene and activates its expression. Xa10 encodes an executor R protein that triggers hypersensitive response and activates disease resistance. ‘Nipponbare’ rice carries two Xa10-like genes in its genome, of which one is the susceptible allele of the Xa23 gene, a Xa10-like TAL effector-dependent executor R gene isolated recently from ‘CBB23’ rice. However, the function of the two Xa10-like genes in disease resistance to X. oryzae pv. oryzae strains has not been investigated. Here, we designated the two Xa10-like genes as Xa10-Ni and Xa23-Ni and characterized their function for disease resistance to rice bacterial blight. Both Xa10-Ni and Xa23-Ni provided disease resistance to X. oryzae pv. oryzae strains that deliver the matching artificially designed TAL effectors (dTALE). Transgenic rice plants containing Xa10-Ni and Xa23-Ni under the Xa10 promoter provided specific disease resistance to X. oryzae pv. oryzae strains that deliver AvrXa10. Xa10-Ni and Xa23-Ni knock-out mutants abolished dTALE-dependent disease resistance to X. oryzae pv. oryzae. Heterologous expression of Xa10-Ni and Xa23-Ni in Nicotiana benthamiana triggered cell death. The 19-amino-acid residues at the N-terminal regions of XA10 or XA10-Ni are dispensable for their function in inducing cell death in N. benthamiana and the C-terminal regions of XA10, XA10-Ni, and XA23-Ni are interchangeable among each other without affecting their function. Like XA10, both XA10-Ni and XA23-Ni locate to the endoplasmic reticulum (ER) membrane, show self-interaction, and induce ER Ca2+ depletion in leaf cells of N. benthamiana. The results indicate that Xa10-Ni and Xa23-Ni in Nipponbare encode functional executor R proteins, which induce cell death in both monocotyledonous and dicotyledonous plants and have the potential of being engineered to provide broad-spectrum disease resistance to plant-pathogenic Xanthomonas spp.

scholarly journals Cytoplasmic and Nuclear Localizations Are Important for the Hypersensitive Response Conferred by Maize Autoactive Rp1-D21 Protein

2015 ◽  
Vol 28 (9) ◽  
pp. 1023-1031 ◽  
Author(s):  
Guan-Feng Wang ◽  
Peter J. Balint-Kurti
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Programmed Cell Death ◽  
Hypersensitive Response ◽  
Nicotiana Benthamiana ◽  
Coiled Coil ◽  
Intragenic Recombination ◽  
R Genes ◽  
Leucine Rich Repeat ◽  
Functional Roles

Disease resistance (R) genes have been isolated from many plant species. Most encode nucleotide binding leucine-rich repeat (NLR) proteins that trigger a rapid localized programmed cell death called the hypersensitive response (HR) upon pathogen recognition. Despite their structural similarities, different NLR are distributed in a range of subcellular locations, and analogous domains play diverse functional roles. The autoactive maize NLR gene Rp1-D21 derives from an intragenic recombination between two NLR genes, Rp1-D and Rp1-dp2, and confers a HR independent of the presence of a pathogen. Rp1-D21 and its N-terminal coiled coil (CC) domain (CCD21) confer autoactive HR when transiently expressed in Nicotiana benthamiana. Rp1-D21 was predominantly localized in cytoplasm with a small amount in the nucleus, while CCD21 was localized in both nucleus and cytoplasm. Targeting of Rp1-D21 or CCD21 predominantly to either the nucleus or the cytoplasm abolished HR-inducing activity. Coexpression of Rp1-D21 or CCD21 constructs confined, respectively, to the nucleus and cytoplasm did not rescue full activity, suggesting nucleocytoplasmic movement was important for HR induction. This work emphasizes the diverse structural and subcellular localization requirements for activity found among plant NLR R genes.

scholarly journals Genome-wide functional analysis of hot pepper immune receptors reveals an autonomous NLR cluster in seed plants

2019 ◽  
Author(s):  
Hye-Young Lee ◽  
Hyunggon Mang ◽  
Eun-Hye Choi ◽  
Ye-Eun Seo ◽  
Myung-Shin Kim ◽  
...  
Keyword(s):  
Cell Death ◽  
Coiled Coil ◽  
Seed Plants ◽  
Hot Pepper ◽  
R Gene ◽  
Leucine Rich Repeat ◽  
Nucleotide Binding Domain ◽  
Immune Receptors ◽  
Genome Wide ◽  
Hr Cell Death

AbstractPlants possess hundreds of intracellular immune receptors encoding nucleotide-binding domain and leucine-rich repeat (NLR) proteins. Autoactive NLRs, in some cases a specific NLR domain, induce plant cell death in the absence of pathogen infection. In this study, we identified a group of NLRs (G10) carrying autoactive coiled-coil (CC) domains in pepper (Capsicum annuum L. cv. CM334) by genome-wide transient expression analysis. The G10-CC-mediated cell death mimics hypersensitive response (HR) cell death triggered by interaction between NLR and effectors derived from pathogens. Sequence alignment and mutagenesis analyses revealed that the intact α1 helix of G10-CCs is critical for both G10-CC- and R gene-mediated HR cell death. The cell death induced by G10-CCs does not require known helper NLRs, suggesting G10-NLRs are novel singleton NLRs. We also found that G10-CCs localize in the plasma membrane as Arabidopsis singleton NLR ZAR1. Extended studies revealed that autoactive G10-CCs are well conserved in other Solanaceae plants, including tomato, potato, and tobacco, as well as a monocot plant, rice. Furthermore, G10-NLR is an ancient form of NLR that present in all tested seed plants (spermatophytes). Our studies not only uncover the autonomous NLR cluster in plants but also provide powerful resources for dissecting the underlying molecular mechanism of NLR-mediated cell death in plants.

scholarly journals Uncoupling Salicylic Acid-Dependent Cell Death and Defense-Related Responses From Disease Resistance in the Arabidopsis Mutant acd5

Genetics ◽  
2000 ◽  
Vol 156 (1) ◽  
pp. 341-350
Author(s):  
Jean T Greenberg ◽  
F Paul Silverman ◽  
Hua Liang
Keyword(s):  
Cell Death ◽  
Salicylic Acid ◽  
Disease Resistance ◽  
Pseudomonas Syringae ◽  
Higher Plants ◽  
Ethylene Signaling ◽  
Symptom Development ◽  
Wild Type ◽  
Dependent Cell ◽  
Arabidopsis Mutant

Abstract Salicylic acid (SA) is required for resistance to many diseases in higher plants. SA-dependent cell death and defense-related responses have been correlated with disease resistance. The accelerated cell death 5 mutant of Arabidopsis provides additional genetic evidence that SA regulates cell death and defense-related responses. However, in acd5, these events are uncoupled from disease resistance. acd5 plants are more susceptible to Pseudomonas syringae early in development and show spontaneous SA accumulation, cell death, and defense-related markers later in development. In acd5 plants, cell death and defense-related responses are SA dependent but they do not confer disease resistance. Double mutants with acd5 and nonexpressor of PR1, in which SA signaling is partially blocked, show greatly attenuated cell death, indicating a role for NPR1 in controlling cell death. The hormone ethylene potentiates the effects of SA and is important for disease symptom development in Arabidopsis. Double mutants of acd5 and ethylene insensitive 2, in which ethylene signaling is blocked, show decreased cell death, supporting a role for ethylene in cell death control. We propose that acd5 plants mimic P. syringae-infected wild-type plants and that both SA and ethylene are normally involved in regulating cell death during some susceptible pathogen infections.

scholarly journals Overexpression of Pto Induces a Salicylate-Independent Cell Death But Inhibits Necrotic Lesions Caused by Salicylate-Deficiency in Tomato Plants

2002 ◽  
Vol 15 (7) ◽  
pp. 654-661 ◽  
Author(s):  
Jianxiong Li ◽  
Libo Shan ◽  
Jian-Min Zhou ◽  
Xiaoyan Tang
Keyword(s):  
Cell Death ◽  
Disease Resistance ◽  
Pseudomonas Syringae ◽  
Virulent Strain ◽  
Gene Activation ◽  
Cellular Damage ◽  
Minor Role ◽  
Disease Resistance Gene ◽  
Tomato Plants ◽  
Spontaneous Cell Death

Tomato plants overexpressing the disease resistance gene Pto (35S∷Pto) exhibit spontaneous cell death, accumulation of salicylic acid (SA), elevated expression of pathogenesis-related genes, and enhanced resistance to a broad range of pathogens. Because salicylate plays an important role in the cell death and defense activation in many lesion mimic mutants, we investigated the interaction of SA-mediated processes and the 35S∷Pto-mediated defense pathway by introducing the nahG transgene that encodes salicylate hydroxylase. Here, we show that SA is not required for the 35S∷Pto-activated microscopic cell death and plays a minor role in defense gene activation and general disease resistance in 35S∷Pto plants. In contrast, temperature greatly affects the spontaneous cell death and general resistance in 35S∷Pto plants, and high temperature inhibits the cell death. The NahG tomato plants develop spontaneous, unconstrained necrotic lesions on leaves. These lesions also are initiated by the inoculation of a virulent strain of Pseudomonas syringae pv. tomato. However, the NahG-dependent necrotic lesions are inhibited in the NahG/35S∷Pto plants. This inhibition is most pronounced under conditions favoring the 35S∷Pto-mediated spontaneous cell death development. These results indicate that the signaling pathways activated by Pto overexpression suppress the cellular damage that is caused by SA depletion. We also found that ethylene is dispensable for the 35S∷Pto-mediated general defense.

scholarly journals Cloning and Characterization of R3b; Members of the R3 Superfamily of Late Blight Resistance Genes Show Sequence and Functional Divergence

2011 ◽  
Vol 24 (10) ◽  
pp. 1132-1142 ◽  
Author(s):  
Guangcun Li ◽  
Sanwen Huang ◽  
Xiao Guo ◽  
Ying Li ◽  
Yu Yang ◽  
...  
Keyword(s):  
Late Blight ◽  
Positional Cloning ◽  
Sequence Similarity ◽  
Functional Divergence ◽  
Durable Resistance ◽  
Coiled Coil ◽  
Avirulence Gene ◽  
R Gene ◽  
Gene Stacking ◽  
High Sequence Similarity

Massive resistance (R) gene stacking is considered to be one of the most promising approaches to provide durable resistance to potato late blight for both conventional and genetically modified breeding strategies. The R3 complex locus on chromosome XI in potato is an example of natural R gene stacking, because it contains two closely linked R genes (R3a and R3b) with distinct resistance specificities to Phytophthora infestans. Here, we report about the positional cloning of R3b. Both transient and stable transformations of susceptible tobacco and potato plants showed that R3b conferred full resistance to incompatible P. infestans isolates. R3b encodes a coiled-coil nucleotide-binding site leucine-rich repeat protein and exhibits 82% nucleotide identity with R3a located in the same R3 cluster. The R3b gene specifically recognizes Avr3b, a newly identified avirulence factor from P. infestans. R3b does not recognize Avr3a, the corresponding avirulence gene for R3a, showing that, despite their high sequence similarity, R3b and R3a have clearly distinct recognition specificities. In addition to the Rpi-mcd1/Rpi-blb3 locus on chromosome IV, the R3 locus on chromosome XI is the second example of an R-gene cluster with multiple genes recognizing different races of P. infestans.

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