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1.
Cell ; 178(5): 1260-1272.e14, 2019 Aug 22.
Artigo em Inglês | MEDLINE | ID: mdl-31442410

RESUMO

Infectious disease is both a major force of selection in nature and a prime cause of yield loss in agriculture. In plants, disease resistance is often conferred by nucleotide-binding leucine-rich repeat (NLR) proteins, intracellular immune receptors that recognize pathogen proteins and their effects on the host. Consistent with extensive balancing and positive selection, NLRs are encoded by one of the most variable gene families in plants, but the true extent of intraspecific NLR diversity has been unclear. Here, we define a nearly complete species-wide pan-NLRome in Arabidopsis thaliana based on sequence enrichment and long-read sequencing. The pan-NLRome largely saturates with approximately 40 well-chosen wild strains, with half of the pan-NLRome being present in most accessions. We chart NLR architectural diversity, identify new architectures, and quantify selective forces that act on specific NLRs and NLR domains. Our study provides a blueprint for defining pan-NLRomes.

2.
Curr Opin Plant Biol ; 50: 82-94, 2019 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-31063902

RESUMO

Plant nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins function as intracellular receptors in response to pathogens and activate effector-triggered immune responses (ETI). The activation of some sensor NLRs (sNLR) by their corresponding pathogen effector is well studied. However, the mechanisms by which the recently defined helper NLRs (hNLR) function to transduce sNLR activation into ETI-associated cell death and disease resistance remains poorly understood. We briefly summarize recent examples of sNLR activation and we then focus on hNLR requirements in sNLR-initiated immune responses. We further discuss how shared sequence homology with fungal self-incompatibility proteins and the mammalian mixed lineage kinase domain like pseudokinase (MLKL) proteins informs a plausible model for the structure and function of an ancient clade of plant hNLRs, called RNLs.

3.
Proc Natl Acad Sci U S A ; 116(7): 2767-2773, 2019 02 12.
Artigo em Inglês | MEDLINE | ID: mdl-30692254

RESUMO

Arabidopsis thaliana accessions are universally resistant at the adult leaf stage to white rust (Albugo candida) races that infect the crop species Brassica juncea and Brassica oleracea We used transgressive segregation in recombinant inbred lines to test if this apparent species-wide (nonhost) resistance in A. thaliana is due to natural pyramiding of multiple Resistance (R) genes. We screened 593 inbred lines from an Arabidopsis multiparent advanced generation intercross (MAGIC) mapping population, derived from 19 resistant parental accessions, and identified two transgressive segregants that are susceptible to the pathogen. These were crossed to each MAGIC parent, and analysis of resulting F2 progeny followed by positional cloning showed that resistance to an isolate of A. candida race 2 (Ac2V) can be explained in each accession by at least one of four genes encoding nucleotide-binding, leucine-rich repeat (NLR) immune receptors. An additional gene was identified that confers resistance to an isolate of A. candida race 9 (AcBoT) that infects B. oleracea Thus, effector-triggered immunity conferred by distinct NLR-encoding genes in multiple A. thaliana accessions provides species-wide resistance to these crop pathogens.


Assuntos
Arabidopsis/imunologia , Brassica/microbiologia , Oomicetos/patogenicidade , Doenças das Plantas/imunologia , Arabidopsis/genética , Arabidopsis/microbiologia , Proteínas de Arabidopsis/genética , Regulação da Expressão Gênica de Plantas , Genes de Plantas , Haplótipos , Imunidade Inata , Doenças das Plantas/microbiologia
4.
Nat Commun ; 10(1): 174, 2019 Jan 08.
Artigo em Inglês | MEDLINE | ID: mdl-30622270

RESUMO

The original version of this article contained an error in the author affiliations. Oliver J. Furzer was incorrectly associated with Department of Plant Sciences, College of Life Sciences, Wuhan University, 430072, Wuhan, China.This has now been corrected in the HTML version of the article. The PDF version of the article was correct at the time of publication.Furthermore, the original version of this article stated that correspondence and requests for materials should be addressed to Heidelberg.Center.for.Personalized.Oncology, DKFZ-HIPO, DKFZ, Heidelberg 69120Germany S.A. (email: shuta.asai@riken.jp) or to J.D.G.J. (email: jonathan.jones@tsl.ac.uk). The words "Heidelberg.Center.for.Personalized.Oncology, DKFZ-HIPO, DKFZ, Heidelberg 69120Germany" were introduced inadvertently.This has now been corrected in the PDF version of the article. The HTML version of the article was correct at the time of publication.

5.
Nat Commun ; 9(1): 5192, 2018 Dec 05.
Artigo em Inglês | MEDLINE | ID: mdl-30518923

RESUMO

Pathogen co-evolution with plants involves selection for evasion of host surveillance systems. The oomycete Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis, and race-specific interactions between Arabidopsis accessions and Hpa isolates fit the gene-for-gene model in which host resistance or susceptibility are determined by matching pairs of plant Resistance (R) genes and pathogen Avirulence (AVR) genes. Arabidopsis Col-0 carries R gene RPP4 that confers resistance to Hpa isolates Emoy2 and Emwa1, but its cognate recognized effector(s) were unknown. We report here the identification of the Emoy2 AVR effector gene recognized by RPP4 and show resistance-breaking isolates of Hpa on RPP4-containing Arabidopsis carry the alleles that either are not expressed, or show cytoplasmic instead of nuclear subcellular localization.

6.
New Phytol ; 2018 Oct 05.
Artigo em Inglês | MEDLINE | ID: mdl-30288750

RESUMO

Physiological races of the oomycete Albugo candida are biotrophic pathogens of diverse plant species, primarily the Brassicaceae, and cause infections that suppress host immunity to other pathogens. However, A. candida race diversity and the consequences of host immunosuppression are poorly understood in the field. We report a method that enables sequencing of DNA of plant pathogens and plant-associated microbes directly from field samples (Pathogen Enrichment Sequencing: PenSeq). We apply this method to explore race diversity in A. candida and to detect A. candida-associated microbes in the field (91 A. candida-infected plants). We show with unprecedented resolution that each host plant species supports colonization by one of 17 distinct phylogenetic lineages, each with an unique repertoire of effector candidate alleles. These data reveal the crucial role of sexual and asexual reproduction, polyploidy and host domestication in A. candida specialization on distinct plant species. Our bait design also enabled phylogenetic assignment of DNA sequences from bacteria and fungi from plants in the field. This paper shows that targeted sequencing has a great potential for the study of pathogen populations while they are colonizing their hosts. This method could be applied to other microbes, especially to those that cannot be cultured.

7.
PLoS Pathog ; 12(8): e1005790, 2016 08.
Artigo em Inglês | MEDLINE | ID: mdl-27513727

RESUMO

Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by 'buzzing' (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts.


Assuntos
Arabidopsis/virologia , Abelhas/fisiologia , Cucumovirus , Lycopersicon esculentum/virologia , Animais , Arabidopsis/fisiologia , Comportamento Alimentar/fisiologia , Cromatografia Gasosa-Espectrometria de Massas , Lycopersicon esculentum/fisiologia , Modelos Teóricos , Doenças das Plantas/virologia , Polinização/fisiologia , Compostos Orgânicos Voláteis/metabolismo
8.
Bioessays ; 38(8): 769-81, 2016 08.
Artigo em Inglês | MEDLINE | ID: mdl-27339076

RESUMO

Intracellular NLR (Nucleotide-binding domain and Leucine-rich Repeat-containing) receptors are sensitive monitors that detect pathogen invasion of both plant and animal cells. NLRs confer recognition of diverse molecules associated with pathogen invasion. NLRs must exhibit strict intramolecular controls to avoid harmful ectopic activation in the absence of pathogens. Recent discoveries have elucidated the assembly and structure of oligomeric NLR signalling complexes in animals, and provided insights into how these complexes act as scaffolds for signal transduction. In plants, recent advances have provided novel insights into signalling-competent NLRs, and into the myriad strategies that diverse plant NLRs use to recognise pathogens. Here, we review recent insights into the NLR biology of both animals and plants. By assessing commonalities and differences between kingdoms, we are able to develop a more complete understanding of NLR function.


Assuntos
Imunidade Inata , Infecção/metabolismo , Proteínas NLR/fisiologia , Plantas/metabolismo , Transdução de Sinais , Animais , Infecção/imunologia , Plantas/imunologia , Plantas/microbiologia
9.
Nat Commun ; 6: 6338, 2015 Mar 06.
Artigo em Inglês | MEDLINE | ID: mdl-25744164

RESUMO

Plant immunity requires recognition of pathogen effectors by intracellular NB-LRR immune receptors encoded by Resistance (R) genes. Most R proteins recognize a specific effector, but some function in pairs that recognize multiple effectors. Arabidopsis thaliana TIR-NB-LRR proteins RRS1-R and RPS4 together recognize two bacterial effectors, AvrRps4 from Pseudomonas syringae and PopP2 from Ralstonia solanacearum. However, AvrRps4, but not PopP2, is recognized in rrs1/rps4 mutants. We reveal an R gene pair that resembles and is linked to RRS1/RPS4, designated as RRS1B/RPS4B, which confers recognition of AvrRps4 but not PopP2. Like RRS1/RPS4, RRS1B/RPS4B proteins associate and activate defence genes upon AvrRps4 recognition. Inappropriate combinations (RRS1/RPS4B or RRS1B/RPS4) are non-functional and this specificity is not TIR domain dependent. Distinct putative orthologues of both pairs are maintained in the genomes of Arabidopsis thaliana relatives and are likely derived from a common ancestor pair. Our results provide novel insights into paired R gene function and evolution.


Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/genética , Proteínas de Bactérias/metabolismo , Imunidade Vegetal/genética , Proteínas de Plantas/metabolismo , Fatores de Transcrição/metabolismo , Arabidopsis/imunologia , Proteínas de Arabidopsis/genética , Mapeamento Cromossômico , Primers do DNA/genética , Evolução Molecular , Immunoblotting , Filogenia , Folhas de Planta/genética , Folhas de Planta/metabolismo , Proteínas/genética , Proteínas/metabolismo , Pseudomonas syringae/genética , Pseudomonas syringae/metabolismo , Ralstonia solanacearum/genética , Ralstonia solanacearum/metabolismo , Reação em Cadeia da Polimerase em Tempo Real , Reação em Cadeia da Polimerase Via Transcriptase Reversa , Especificidade da Espécie , Fatores de Transcrição/genética
10.
Mol Plant Pathol ; 16(4): 413-34, 2015 May.
Artigo em Inglês | MEDLINE | ID: mdl-25178392

RESUMO

Oomycetes form a deep lineage of eukaryotic organisms that includes a large number of plant pathogens which threaten natural and managed ecosystems. We undertook a survey to query the community for their ranking of plant-pathogenic oomycete species based on scientific and economic importance. In total, we received 263 votes from 62 scientists in 15 countries for a total of 33 species. The Top 10 species and their ranking are: (1) Phytophthora infestans; (2, tied) Hyaloperonospora arabidopsidis; (2, tied) Phytophthora ramorum; (4) Phytophthora sojae; (5) Phytophthora capsici; (6) Plasmopara viticola; (7) Phytophthora cinnamomi; (8, tied) Phytophthora parasitica; (8, tied) Pythium ultimum; and (10) Albugo candida. This article provides an introduction to these 10 taxa and a snapshot of current research. We hope that the list will serve as a benchmark for future trends in oomycete research.


Assuntos
Oomicetos/classificação , Plantas/microbiologia , Oomicetos/patogenicidade
11.
PLoS Pathog ; 10(10): e1004443, 2014 Oct.
Artigo em Inglês | MEDLINE | ID: mdl-25329884

RESUMO

Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.


Assuntos
Arabidopsis/efeitos dos fármacos , Arabidopsis/genética , Interações Hospedeiro-Patógeno/imunologia , Oomicetos/efeitos dos fármacos , Doenças das Plantas/imunologia , Imunidade Vegetal/imunologia , Ácido Salicílico/farmacologia , Proteínas de Arabidopsis/genética , Sequência de Bases/genética , Regulação da Expressão Gênica de Plantas , Interações Hospedeiro-Patógeno/efeitos dos fármacos , Oomicetos/genética , Doenças das Plantas/genética , Doenças das Plantas/microbiologia , Ácido Salicílico/metabolismo
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