scholarly journals Harnessing Effector-Triggered Immunity for Durable Disease Resistance

2017 ◽  
Vol 107 (8) ◽  
pp. 912-919 ◽  
Author(s):  
Meixiang Zhang ◽  
Gitta Coaker
Keyword(s):  
Disease Resistance ◽  
Plant Pathogens ◽  
Domain Architecture ◽  
Effector Proteins ◽  
Plant Diseases ◽  
Sources Of Resistance ◽  
Pathogen Effectors ◽  
Pathogen Effector ◽  
Effector Triggered Immunity ◽  
Durable Disease Resistance

Genetic control of plant diseases has traditionally included the deployment of single immune receptors with nucleotide-binding leucine-rich repeat (NLR) domain architecture. These NLRs recognize corresponding pathogen effector proteins inside plant cells, resulting in effector-triggered immunity (ETI). Although ETI triggers robust resistance, deployment of single NLRs can be rapidly overcome by pathogen populations within a single or a few growing seasons. In order to generate more durable disease resistance against devastating plant pathogens, a multitiered strategy that incorporates stacked NLRs combined with other sources of disease resistance is necessary. New genetic and genomic technologies have enabled advancements in identifying conserved pathogen effectors, isolating NLR repertoires from diverse plants, and editing plant genomes to enhance resistance. Significant advancements have also been made in understanding plant immune perception at the receptor level, which has promise for engineering new sources of resistance. Here, we discuss how to utilize recent scientific advancements in a multilayered strategy for developing more durable disease resistance.

scholarly journals Sustained Incompatibility between MAPK Signaling and Pathogen Effectors

2020 ◽  
Vol 21 (21) ◽  
pp. 7954
Author(s):  
Julien Lang ◽  
Jean Colcombet
Keyword(s):  
Defense Responses ◽  
Mapk Signaling ◽  
Effector Proteins ◽  
Plant Defense Responses ◽  
Pathogen Effectors ◽  
Current State ◽  
Pathogen Effector ◽  
Mitogen Activated Protein ◽  
Effector Triggered Immunity ◽  
Signaling Components

In plants, Mitogen-Activated Protein Kinases (MAPKs) are important signaling components involved in developemental processes as well as in responses to biotic and abiotic stresses. In this review, we focus on the roles of MAPKs in Effector-Triggered Immunity (ETI), a specific layer of plant defense responses dependent on the recognition of pathogen effector proteins. Having inspected the literature, we synthesize the current state of knowledge concerning this topic. First, we describe how pathogen effectors can manipulate MAPK signaling to promote virulence, and how in parallel plants have developed mechanisms to protect themselves against these interferences. Then, we discuss the striking finding that the recognition of pathogen effectors can provoke a sustained activation of the MAPKs MPK3/6, extensively analyzing its implications in terms of regulation and functions. In line with this, we also address the question of how a durable activation of MAPKs might affect the scope of their substrates, and thereby mediate the emergence of possibly new ETI-specific responses. By highlighting the sometimes conflicting or missing data, our intention is to spur further research in order to both consolidate and expand our understanding of MAPK signaling in immunity.

The role of oomycete effectors in plant - pathogen interactions

2010 ◽  
Vol 37 (10) ◽  
pp. 919 ◽  
Author(s):  
Adrienne R. Hardham ◽  
David M. Cahill
Keyword(s):  
Plant Cell ◽  
Plant Pathogens ◽  
Plant Defence ◽  
Effector Proteins ◽  
Plant Structure ◽  
Cell Wall Degrading Enzymes ◽  
Cell Cytoplasm ◽  
Diverse Range ◽  
Successful Infection ◽  
Pathogen Effector

Plants constantly come into contact with a diverse range of microorganisms that are potential pathogens, and they have evolved multi-faceted physical and chemical strategies to inhibit pathogen ingress and establishment of disease. Microbes, however, have developed their own strategies to counteract plant defence responses. Recent research on plant–microbe interactions has revealed that an important part of the infection strategies of a diverse range of plant pathogens, including bacteria, fungi and oomycetes, is the production of effector proteins that are secreted by the pathogen and that promote successful infection by manipulating plant structure and metabolism, including interference in plant defence mechanisms. Pathogen effector proteins may function either in the extracellular spaces within plant tissues or within the plant cell cytoplasm. Extracellular effectors include cell wall degrading enzymes and inhibitors of plant enzymes that attack invading pathogens. Intracellular effectors move into the plant cell cytoplasm by as yet unknown mechanisms where, in incompatible interactions, they may be recognised by plant resistance proteins but where, in compatible interactions, they may suppress the plant’s immune response. This article presents a brief overview of our current understanding of the nature and function of effectors produced by oomycete plant pathogens.

scholarly journals Molecular mechanisms of host cell manipulation by plant pathogens

2014 ◽  
Vol 70 (a1) ◽  
pp. C801-C801
Author(s):  
Richard Hughes ◽  
Stuart King ◽  
Abbas Maqbool ◽  
Hazel McLellan ◽  
Tolga Bozkurt ◽  
...  
Keyword(s):  
Cell Death ◽  
Crop Production ◽  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Complex Structure ◽  
Effector Proteins ◽  
Plant Diseases ◽  
Cell Manipulation ◽  
Cell Physiology ◽  
Structural Studies

An estimated 15% of global crop production is lost to pre-harvest disease every year. New ways to manage plant diseases are required. A mechanistic understanding of how plant pathogens re-program their hosts to enable colonisation may provide novel genetic or chemical opportunities to interfere with disease. One notorious plant parasite is the Irish potato famine pathogen Phytophthora infestans. This pathogen remains a considerable threat to potato/tomato crops today as the agent of late blight. Plant pathogens secrete effector proteins outside of and into plant cells to suppress host defences and manipulate cell physiology. Structural studies have provided insights into effector evolution and enabled experiments to probe function [1-3]. Crystal structures of 4 Phytophthora RXLR-type effectors, which are unrelated in primary sequence, revealed similarities in the fold of these proteins. This fold was proposed to act as a stable scaffold that supports diversification of effectors. Further, molecular modelling has enabled mapping of single-site variants responsible for specialisation of a Phytophthora Cystatin-like effector, revealing how effectors can adapt to new hosts after a "host jump". Structural studies describing how RXLR-effectors interact with host targets are lacking. We have used Y2H/co-IP studies to identify host proteins that interact with P. infestans effectors PexRD2 and PexRD54. PexRD2 interacts with MAPKKKe, a component of plant immune signalling pathways, and suppressed cell death activities of this protein. We used the structure of PexRD2 to design mutants that fail to interact with MAPKKKe, and no longer suppress cell-death activities. We found that PexRD54 interacts with potato homologues of the autophagy protein ATG8. We have obtained a crystal structure for PexRD54 in the presence of ATG8. We are now using X-ray scattering to verify the complex structure in solution prior to establishing the role of this interaction during infection.

scholarly journals The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence

2010 ◽  
Vol 107 (5) ◽  
pp. 2349-2354 ◽  
Author(s):  
Mike Wilton ◽  
Rajagopal Subramaniam ◽  
James Elmore ◽  
Corinna Felsensteiner ◽  
Gitta Coaker ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Immunity ◽  
Effector Proteins ◽  
Type Iii ◽  
Pathogen Effector ◽  
Effector Triggered Immunity ◽  
Type Iii Secretion Effector ◽  
Virulence Target

Plant immunity can be induced by two major classes of pathogen-associated molecules. Pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) are conserved molecular components of microbes that serve as “non-self” features to induce PAMP-triggered immunity (PTI). Pathogen effector proteins used to promote virulence can also be recognized as “non-self” features or induce a “modified-self” state that can induce effector-triggered immunity (ETI). The Arabidopsis protein RIN4 plays an important role in both branches of plant immunity. Three unrelated type III secretion effector (TTSE) proteins from the phytopathogen Pseudomonas syringae, AvrRpm1, AvrRpt2, and AvrB, target RIN4, resulting in ETI that effectively restricts pathogen growth. However, no pathogenic advantage has been demonstrated for RIN4 manipulation by these TTSEs. Here, we show that the TTSE HopF2Pto also targets Arabidopsis RIN4. Transgenic plants conditionally expressing HopF2Pto were compromised for AvrRpt2-induced RIN4 modification and associated ETI. HopF2Pto interfered with AvrRpt2-induced RIN4 modification in vitro but not with AvrRpt2 activation, suggestive of RIN4 targeting by HopF2Pto. In support of this hypothesis, HopF2Pto interacted with RIN4 in vitro and in vivo. Unlike AvrRpm1, AvrRpt2, and AvrB, HopF2Pto did not induce ETI and instead promoted P. syringae growth in Arabidopsis. This virulence activity was not observed in plants genetically lacking RIN4. These data provide evidence that RIN4 is a major virulence target of HopF2Pto and that a pathogenic advantage can be conveyed by TTSEs that target RIN4.

scholarly journals Accurate plant pathogen effector protein classification ab initio with deepredeff: an ensemble of convolutional neural networks

2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Ruth Kristianingsih ◽  
Dan MacLean
Keyword(s):  
Neural Networks ◽  
Deep Learning ◽  
Convolutional Neural Networks ◽  
Plant Pathogens ◽  
De Novo ◽  
Chemical Properties ◽  
Effector Proteins ◽  
Global Food Security ◽  
Pathogen Effector ◽  
Biological Insight

Abstract Background Plant pathogens cause billions of dollars of crop loss every year and are a major threat to global food security. Effector proteins are the tools such pathogens use to infect the cell, predicting effectors de novo from sequence is difficult because of the heterogeneity of the sequences. We hypothesised that deep learning classifiers based on Convolutional Neural Networks would be able to identify effectors and deliver new insights. Results We created a training set of manually curated effector sequences from PHI-Base and used these to train a range of model architectures for classifying bacteria, fungal and oomycete sequences. The best performing classifiers had accuracies from 93 to 84%. The models were tested against popular effector detection software on our own test data and data provided with those models. We observed better performance from our models. Specifically our models showed greater accuracy and lower tendencies to call false positives on a secreted protein negative test set and a greater generalisability. We used GRAD-CAM activation map analysis to identify the sequences that activated our CNN-LSTM models and found short but distinct N-terminal regions in each taxon that was indicative of effector sequences. No motifs could be observed in these regions but an analysis of amino acid types indicated differing patterns of enrichment and depletion that varied between taxa. Conclusions Small training sets can be used effectively to train highly accurate and sensitive deep learning models without need for the operator to know anything other than sequence and without arbitrary decisions made about what sequence features or physico-chemical properties are important. Biological insight on subsequences important for classification can be achieved by examining the activations in the model

scholarly journals Structural requirements of the phytoplasma effector protein SAP54 for causing homeotic transformation of floral organs

2019 ◽  
Author(s):  
Marc-Benjamin Aurin ◽  
Michael Haupt ◽  
Matthias Görlach ◽  
Florian Rümpler ◽  
Günter Theißen
Keyword(s):  
Plant Pathogens ◽  
Ornamental Plants ◽  
Effector Proteins ◽  
Plant Diseases ◽  
Scattering Data ◽  
Effector Protein ◽  
Homeotic Transformation ◽  
Structural Requirements ◽  
Floral Organs ◽  
Floral Homeotic

SummaryPhytoplasmas are intracellular bacterial plant pathogens that cause devastating diseases in crops and ornamental plants by the secretion of effector proteins. One of these effector proteins, termed SECRETED ASTER YELLOWS-WITCHES’ BROOM PROTEIN 54 (SAP54), leads to the degradation of a specific subset of floral homeotic proteins of the MIKC-type MADS-domain family via the ubiquitin-proteasome pathway. In consequence, the developing flowers show the homeotic transformation of floral organs into vegetative leaf-like structures. The molecular mechanism of SAP54 action involves physical binding to the keratin-like K-domain of MIKC-type proteins, and to some RAD23 proteins, which translocate ubiquitylated substrates to the proteasome. The structural requirements and specificity of SAP54 function are poorly understood, however. Here we report, based on biophysical and molecular biological analyses, that SAP54 folds into α-helical structures. We also show that the insertion of helix-breaking mutations disrupts correct folding of SAP54, which interferes with the ability of SAP54 to bind to its target proteins and to cause disease phenotypes in vivo. Surprisingly, dynamic light scattering data together with electrophoretic mobility shift assays suggest that SAP54 preferentially binds to multimeric complexes of MIKC-type proteins rather than to dimers or monomers of these proteins. Together with literature data this finding suggests that MIKC-type proteins and SAP54 constitute multimeric α-helical coiled-coils, possibly also involving other partners such as RAD23 proteins. Our investigations clarify the structure-function relationship of an important phytoplasma effector protein and thus may ultimately help to develop treatments against some devastating plant diseases.SIGNIFICANCE STATEMENTPhytoplasmas are bacterial plant pathogens that cause devastating diseases in crops and ornamental plants by the secretion of effector proteins such as SAP54, which leads to the degradation of some floral homeotic proteins. Our study clarifies the structural requirements of SAP54 function and illuminates the molecular mode of interaction and thus may ultimately help to develop treatments against some devastating plant diseases.

scholarly journals Structural Requirements of the Phytoplasma Effector Protein SAP54 for Causing Homeotic Transformation of Floral Organs

2020 ◽  
Vol 33 (9) ◽  
pp. 1129-1141
Author(s):  
Marc-Benjamin Aurin ◽  
Michael Haupt ◽  
Matthias Görlach ◽  
Florian Rümpler ◽  
Günter Theißen
Keyword(s):  
Plant Pathogens ◽  
Effector Proteins ◽  
Plant Diseases ◽  
Scattering Data ◽  
Effector Protein ◽  
Mobility Shift ◽  
Homeotic Transformation ◽  
Structural Requirements ◽  
Floral Organs ◽  
Specific Subset

Phytoplasmas are intracellular bacterial plant pathogens that cause devastating diseases in crops and ornamental plants by the secretion of effector proteins. One of these effector proteins, termed SECRETED ASTER YELLOWS WITCHES’ BROOM PROTEIN 54 (SAP54), leads to the degradation of a specific subset of floral homeotic proteins of the MIKC-type MADS-domain family via the ubiquitin-proteasome pathway. In consequence, the developing flowers show the homeotic transformation of floral organs into vegetative leaf-like structures. The molecular mechanism of SAP54 action involves binding to the keratin-like domain of MIKC-type proteins and to some RAD23 proteins, which translocate ubiquitylated substrates to the proteasome. The structural requirements and specificity of SAP54 function are poorly understood, however. Here, we report, based on biophysical and molecular biological analyses, that SAP54 folds into an α-helical structure. Insertion of helix-breaking mutations disrupts correct folding of SAP54 and compromises SAP54 binding to its target proteins and, concomitantly, its ability to evoke disease phenotypes in vivo. Interestingly, dynamic light scattering data together with electrophoretic mobility shift assays suggest that SAP54 preferentially binds to multimeric complexes of MIKC-type proteins rather than to dimers or monomers of these proteins. Together with data from literature, this finding suggests that MIKC-type proteins and SAP54 constitute multimeric α-helical coiled coils. Our investigations clarify the structure-function relationship of an important phytoplasma effector protein and may thus ultimately help to develop treatments against some devastating plant diseases.

scholarly journals Recognitional Specificity and Evolution in the Tomato–Cladosporium fulvum Pathosystem

2009 ◽  
Vol 22 (10) ◽  
pp. 1191-1202 ◽  
Author(s):  
B. B. H. Wulff ◽  
A. Chakrabarti ◽  
D. A. Jones
Keyword(s):  
Defense Mechanisms ◽  
Extracellular Proteins ◽  
Effector Proteins ◽  
Cladosporium Fulvum ◽  
Host Proteins ◽  
Pathogen Effectors ◽  
Passalora Fulva ◽  
Pathogen Effector ◽  
Mold Fungus ◽  
Avr Genes

The interactions between plants and many biotrophic or hemibiotrophic pathogens are controlled by receptor proteins in the host and effector proteins delivered by the pathogen. Pathogen effectors facilitate pathogen growth through the suppression of host defenses and the manipulation of host metabolism, but recognition of a pathogen-effector protein by a host receptor enables the host to activate a suite of defense mechanisms that limit pathogen growth. In the tomato (Lycopersicon esculentum syn. Solanum lycopersicum)–Cladosporium fulvum (leaf mold fungus syn. Passalora fulva) pathosystem, the host receptors are plasma membrane–anchored, leucine-rich repeat, receptor-like proteins encoded by an array of Cf genes conferring resistance to C. fulvum. The pathogen effectors are mostly small, secreted, cysteine-rich, but otherwise largely dissimilar, extracellular proteins encoded by an array of avirulence (Avr) genes, so called because of their ability to trigger resistance and limit pathogen growth when the corresponding Cf gene is present in tomato. A number of Cf and Avr genes have been isolated, and details of the complex molecular interplay between tomato Cf proteins and C. fulvum effector proteins are beginning to emerge. Each effector appears to have a different role; probably most bind or modify different host proteins, but at least one has a passive role masking the pathogen. It is, therefore, not surprising that each effector is probably detected in a distinct and specific manner, some by direct binding, others as complexes with host proteins, and others via their modification of host proteins. The two papers accompanying this review contribute further to our understanding of the molecular specificity underlying effector perception by Cf proteins. This review, therefore, focuses on our current understanding of recognitional specificity in the tomato–C. fulvum pathosystem and highlights some of the critical questions that remain to be addressed. It also addresses the evolutionary causes and consequences of this specificity.

scholarly journals Accurate plant pathogen effector protein classification ab initio with deepredeff, an ensemble of convolutional neural networks

2020 ◽  
Author(s):  
Ruth Kristianingsih ◽  
Dan MacLean
Keyword(s):  
Neural Networks ◽  
Convolutional Neural Networks ◽  
Plant Pathogens ◽  
De Novo ◽  
R Package ◽  
Effector Proteins ◽  
Global Food Security ◽  
Pathogen Effector ◽  
Detection Software ◽  
Map Analysis

Plant pathogens cause billions of dollars of crop loss every year and are a major threat to global food security. Effector proteins are the tools such pathogens use to infect the cell, predicting effectors de novo from sequence is difficult because of the heterogeneity of the sequences. We hypothesised that deep learning classifiers based on Convolutional Neural Networks would be able to identify effectors and deliver new insights. We built a training set of manually curated effector sequences from PHI-Base and used these to train a range of model architectures for classifying bacteria, fungal and oomycete sequences. The best performing classifiers had accuracies from 93 % to 84 %. The models were tested against popular effector detection software on our own test data and data provided with those models. We observed better performance from our models. Specifically our models showed greater accuracy and lower tendencies to call false positives on a secreted protein negative test set and a greater generalisability. We used GRAD-CAM activation map analysis to identify the sequences that activated our CNN-LSTM models and found short but distinct N-terminal regions in each taxon that was indicative of effector sequences. No motifs could be observed in these regions but an analysis of amino acid types indicated differing patterns of enrichment and depletion that varied between taxa. We have produced an R package that will allow others to make easy effector predictions using our models.

scholarly journals Roq1 confers resistance to Xanthomonas, Pseudomonas syringae and Ralstonia solanacearum in tomato

2019 ◽  
Author(s):  
Nicholas C. Thomas ◽  
Connor G. Hendrich ◽  
Upinder S. Gill ◽  
Caitilyn Allen ◽  
Samuel F. Hutton ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Ralstonia Solanacearum ◽  
Plant Pathogens ◽  
Field Trials ◽  
Current Control ◽  
Effector Proteins ◽  
Effective Control ◽  
Crop Species ◽  
Xanthomonas Perforans ◽  
Pathogen Effector

AbstractXanthomonas species, Pseudomonas syringae and Ralstonia solanacearum are bacterial plant pathogens that cause significant yield loss in many crop species. Current control methods for these pathogens are insufficient but there is significant potential for generating new disease-resistant crop varieties. Plant immune receptors encoded by nucleotide-binding, leucine-rich repeat (NLR) genes typically confer resistance to pathogens that produce a cognate elicitor, often an effector protein secreted by the pathogen to promote virulence. The diverse sequence and presence / absence variation of pathogen effector proteins within and between pathogen species usually limits the utility of a single NLR gene to protecting a plant from a single pathogen species or particular strains. The NLR protein Recognition of XopQ 1 (Roq1) was recently identified from the plant Nicotiana benthamiana and mediates perception of the effector proteins XopQ and HopQ1 from Xanthomonas and P. syringae respectively. Unlike most recognized effectors, alleles of XopQ/HopQ1 are highly conserved and present in most plant pathogenic strains of Xanthomonas and P. syringae. A homolog of XopQ/HopQ1, named RipB, is present in many R. solanacearum strains. We found that Roq1 also mediates perception of RipB and confers immunity to Xanthomonas, P. syringae, and R. solanacearum when expressed in tomato. Strong resistance to Xanthomonas perforans was observed in three seasons of field trials with both natural and artificial inoculation. The Roq1 gene can therefore be used to provide safe, economical and effective control of these pathogens in tomato and other crop species and reduce or eliminate the need for traditional chemical controls.SummaryA single immune receptor expressed in tomato confers strong resistance to three different bacterial diseases.

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