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Article ; Online: Effector-Decoy Pairs: Another Countermeasure Emerging during Host-Microbe Co-evolutionary Arms Races?

Cummins, Michael / Huitema, Edgar

2017 Volume 10, Issue 5, Page(s) 662–664

MeSH term(s)	Evolution, Molecular ; Host-Pathogen Interactions/genetics ; Phytophthora/pathogenicity ; Plants/microbiology ; Proteins/metabolism ; Virulence
Chemical Substances	Proteins
Language	English
Publishing date	2017-03-30
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2393618-6
ISSN	1752-9867 ; 1674-2052
ISSN (online)	1752-9867
ISSN	1674-2052
DOI	10.1016/j.molp.2017.03.008
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Article: A Conserved Oomycete CRN Effector Targets Tomato TCP14-2 to Enhance Virulence.

Stam, Remco / Motion, Graham B / Martinez-Heredia, Victor / Boevink, Petra C / Huitema, Edgar

Molecular plant-microbe interactions : MPMI

2021 Volume 34, Issue 3, Page(s) 309–318

Abstract: ... ...

Abstract	Phytophthora
MeSH term(s)	Lycopersicon esculentum/parasitology ; Phytophthora/genetics ; Phytophthora/pathogenicity ; Plant Diseases/parasitology ; Plant Proteins/metabolism ; Receptors, Cell Surface/metabolism ; Virulence/genetics
Chemical Substances	Plant Proteins ; Receptors, Cell Surface
Language	English
Publishing date	2021-03-03
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-06-20-0172-R
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Article ; Online: Virulence strategies of an insect herbivore and oomycete plant pathogen converge on host E3 SUMO ligase SIZ1.

Liu, Shan / Lenoir, Camille J G / Amaro, Tiago M M M / Rodriguez, Patricia A / Huitema, Edgar / Bos, Jorunn I B

The New phytologist

2022 Volume 235, Issue 4, Page(s) 1599–1614

Abstract: Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence ... ...

Abstract	Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence strategies is largely unexplored. We found that effectors from the oomycete pathogen, Phytophthora capsici, and the major aphid pest, Myzus persicae target the host immune regulator SIZ1, an E3 SUMO ligase. We used transient expression assays in Nicotiana benthamiana as well as Arabidopsis mutants to further characterize biological role of effector-SIZ1 interactions in planta. We show that the oomycete and aphid effector, which both contribute to virulence, feature different activities towards SIZ1. While M. persicae effector Mp64 increases SIZ1 protein levels in transient assays, P. capsici effector CRN83_152 enhances SIZ1-E3 SUMO ligase activity in vivo. SIZ1 contributes to host susceptibility to aphids and an oomycete pathogen. Knockout of SIZ1 in Arabidopsis decreased susceptibility to aphids, independent of SNC1, PAD4 and EDS1. Similarly SIZ1 knockdown in N. benthamiana led to reduced P. capsici infection. Our results suggest convergence of distinct pathogen and pest virulence strategies on an E3 SUMO ligase to enhance host susceptibility.
MeSH term(s)	Animals ; Aphids/metabolism ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Gene Expression Regulation, Plant ; Herbivory ; Ligases/metabolism ; Phytophthora/metabolism ; Ubiquitin-Protein Ligases/metabolism ; Virulence
Chemical Substances	Arabidopsis Proteins ; SNC1 protein, Arabidopsis ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; Ligases (EC 6.-) ; SIZ1 protein, Arabidopsis (EC 6.3.2.-)
Language	English
Publishing date	2022-05-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18184
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Article: Virulence strategies of an insect herbivore and oomycete plant pathogen converge on host E3 SUMO ligase SIZ1

Liu, Shan / Lenoir, Camille J. G. / Amaro, Tiago M. M. M. / Rodriguez, Patricia A. / Huitema, Edgar / Bos, Jorunn I. B.

The new phytologist. 2022 Aug., v. 235, no. 4

2022

Abstract	Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence strategies is largely unexplored. We found that effectors from the oomycete pathogen, Phytophthora capsici, and the major aphid pest, Myzus persicae target the host immune regulator SIZ1, an E3 SUMO ligase. We used transient expression assays in Nicotiana benthamiana as well as Arabidopsis mutants to further characterize biological role of effector–SIZ1 interactions in planta. We show that the oomycete and aphid effector, which both contribute to virulence, feature different activities towards SIZ1. While M. persicae effector Mp64 increases SIZ1 protein levels in transient assays, P. capsici effector CRN83_152 enhances SIZ1‐E3 SUMO ligase activity in vivo. SIZ1 contributes to host susceptibility to aphids and an oomycete pathogen. Knockout of SIZ1 in Arabidopsis decreased susceptibility to aphids, independent of SNC1, PAD4 and EDS1. Similarly SIZ1 knockdown in N. benthamiana led to reduced P. capsici infection. Our results suggest convergence of distinct pathogen and pest virulence strategies on an E3 SUMO ligase to enhance host susceptibility.
Keywords	Arabidopsis ; Myzus persicae ; Nicotiana benthamiana ; Phytophthora capsici ; immunity ; ligases ; phytophagous insects ; plant pathogens ; virulence
Language	English
Dates of publication	2022-08
Size	p. 1599-1614.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18184
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Effector-triggered post-translational modifications and their role in suppression of plant immunity.

Howden, Andrew J M / Huitema, Edgar

Frontiers in plant science

2012 Volume 3, Page(s) 160

Abstract: Plant-pathogen interactions feature complex signaling exchanges between host and microbes that ultimately determine association outcomes. Plants deploy pattern recognition receptors to perceive pathogen-associated molecular patterns, mount pattern- ... ...

Abstract	Plant-pathogen interactions feature complex signaling exchanges between host and microbes that ultimately determine association outcomes. Plants deploy pattern recognition receptors to perceive pathogen-associated molecular patterns, mount pattern-triggered immunity (PTI), and fend off potential pathogens. In recent years an increasing number of defense-signaling components have been identified along with a mechanistic understanding of their regulation during immune responses. Post-translational modifications (PTMs) are now thought to play a crucial role in regulating defense signaling. In a bid to suppress PTI and infect their host, pathogens have evolved large repertoires of effectors that trigger susceptibility and allow colonization of host tissues. While great progress has been made in elucidating defense-signaling networks in plants and the activities of effectors in immune suppression, a critical gap exists in our understanding of effector mechanism-of-action. Given the importance of PTMs in the regulation of defense signaling, we will explore the question: how do effectors modify the post-translational status of host proteins and thus interfere with host processes required for immunity? We will consider how emerging proteomics-based experimental strategies may help us answer this important question and ultimately open the pathogens' effector black box.
Language	English
Publishing date	2012-07-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X ; 1664-462X
ISSN (online)	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2012.00160
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Article: An NMRA-Like Protein Regulates Gene Expression in Phytophthora capsici to Drive the Infection Cycle on Tomato.

Pham, Jasmine / Stam, Remco / Heredia, Victor Martinez / Csukai, Michael / Huitema, Edgar

Molecular plant-microbe interactions : MPMI

2018 Volume 31, Issue 6, Page(s) 665–677

Abstract: Phytophthora spp. cause devastating disease epidemics on important crop plants and pose a grave threat to global crop production. Critically, Phytophthora pathogens represent a distinct evolutionary lineage in which pathogenicity has been acquired ... ...

Abstract	Phytophthora spp. cause devastating disease epidemics on important crop plants and pose a grave threat to global crop production. Critically, Phytophthora pathogens represent a distinct evolutionary lineage in which pathogenicity has been acquired independently. Therefore, there is an urgent need to understand and disrupt the processes that drive infection if we aspire to defeat oomycete pathogens in the field. One area that has received little attention thus far in this respect is the regulation of Phytophthora gene expression during infection. Here, we characterize PcNMRAL1 (Phyca11_505845), a homolog of the Aspergillus nidulans nitrogen metabolite repression regulator NMRA and demonstrate a role for this protein in progression of the Phytophthora capsici infection cycle. PcNmrAL1 is coexpressed with the biotrophic marker gene PcHmp1 (haustorial membrane protein 1) and, when overexpressed, extends the biotrophic infection stage. Microarray analyses revealed that PcNmrAL1 overexpression in P. capsici leads to large-scale transcriptional changes during infection and in vitro. Importantly, detailed analysis reveals that PcNmrAL1 overexpression induces biotrophy-associated genes while repressing those associated with necrotrophy. In addition to factors controlling transcription, translation, and nitrogen metabolism, PcNMRAL1 helps regulate the expression of a considerable effector repertoire in P. capsici. Our data suggests that PcNMRAL1 is a transcriptional regulator that mediates the biotrophy to necrotrophy transition. PcNMRAL1 represents a novel factor that may drive the Phytophthora disease cycle on crops. This study provides the first insight into mechanisms that regulate infection-related processes in Phytophthora spp. and provides a platform for further studies aimed at disabling pathogenesis and preventing crop losses.
MeSH term(s)	Amino Acid Sequence ; Biomarkers ; Gene Expression Profiling ; Gene Expression Regulation, Fungal/physiology ; Lycopersicon esculentum/microbiology ; Phytophthora/genetics ; Phytophthora/metabolism ; Plant Diseases/microbiology ; Proteins/metabolism
Chemical Substances	Biomarkers ; Proteins
Language	English
Publishing date	2018
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-07-17-0193-R
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Article ; Online: DNA-binding protein prediction using plant specific support vector machines: validation and application of a new genome annotation tool.

Motion, Graham B / Howden, Andrew J M / Huitema, Edgar / Jones, Susan

Nucleic acids research

2015 Volume 43, Issue 22, Page(s) e158

Abstract: There are currently 151 plants with draft genomes available but levels of functional annotation for putative protein products are low. Therefore, accurate computational predictions are essential to annotate genomes in the first instance, and to provide ... ...

Abstract	There are currently 151 plants with draft genomes available but levels of functional annotation for putative protein products are low. Therefore, accurate computational predictions are essential to annotate genomes in the first instance, and to provide focus for the more costly and time consuming functional assays that follow. DNA-binding proteins are an important class of proteins that require annotation, but current computational methods are not applicable for genome wide predictions in plant species. Here, we explore the use of species and lineage specific models for the prediction of DNA-binding proteins in plants. We show that a species specific support vector machine model based on Arabidopsis sequence data is more accurate (accuracy 81%) than a generic model (74%), and based on this we develop a plant specific model for predicting DNA-binding proteins. We apply this model to the tomato proteome and demonstrate its ability to perform accurate high-throughput prediction of DNA-binding proteins. In doing so, we have annotated 36 currently uncharacterised proteins by assigning a putative DNA-binding function. Our model is publically available and we propose it be used in combination with existing tools to help increase annotation levels of DNA-binding proteins encoded in plant genomes.
MeSH term(s)	Arabidopsis/genetics ; DNA-Binding Proteins/chemistry ; DNA-Binding Proteins/genetics ; Genome, Plant ; Lycopersicon esculentum/genetics ; Models, Biological ; Molecular Sequence Annotation ; Plant Proteins/chemistry ; Plant Proteins/genetics ; Sequence Analysis, Protein ; Species Specificity ; Support Vector Machine
Chemical Substances	DNA-Binding Proteins ; Plant Proteins
Language	English
Publishing date	2015-08-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Validation Study
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkv805
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Article ; Online: Nuclear processes associated with plant immunity and pathogen susceptibility.

Motion, Graham B / Amaro, Tiago M M M / Kulagina, Natalja / Huitema, Edgar

Briefings in functional genomics

2015 Volume 14, Issue 4, Page(s) 243–252

Abstract: Plants are sessile organisms that have evolved exquisite and sophisticated mechanisms to adapt to their biotic and abiotic environment. Plants deploy receptors and vast signalling networks to detect, transmit and respond to a given biotic threat by ... ...

Abstract	Plants are sessile organisms that have evolved exquisite and sophisticated mechanisms to adapt to their biotic and abiotic environment. Plants deploy receptors and vast signalling networks to detect, transmit and respond to a given biotic threat by inducing properly dosed defence responses. Genetic analyses and, more recently, next-generation -omics approaches have allowed unprecedented insights into the mechanisms that drive immunity. Similarly, functional genomics and the emergence of pathogen genomes have allowed reciprocal studies on the mechanisms governing pathogen virulence and host susceptibility, collectively allowing more comprehensive views on the processes that govern disease and resistance. Among others, the identification of secreted pathogen molecules (effectors) that modify immunity-associated processes has changed the plant-microbe interactions conceptual landscape. Effectors are now considered both important factors facilitating disease and novel probes, suited to study immunity in plants. In this review, we will describe the various mechanisms and processes that take place in the nucleus and help regulate immune responses in plants. Based on the premise that any process required for immunity could be targeted by pathogen effectors, we highlight and describe a number of functional assays that should help determine effector functions and their impact on immune-related processes. The identification of new effector functions that modify nuclear processes will help dissect nuclear signalling further and assist us in our bid to bolster immunity in crop plants.
MeSH term(s)	Alternative Splicing ; Cell Nucleus/physiology ; Chromatin Assembly and Disassembly ; Genome, Plant ; Plants/genetics ; Plants/immunology ; Plants/microbiology ; Protein Processing, Post-Translational ; RNA Processing, Post-Transcriptional ; Transcription, Genetic
Language	English
Publishing date	2015-04-06
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2540916-5
ISSN	2041-2657 ; 2041-2649 ; 2041-2647
ISSN (online)	2041-2657
ISSN	2041-2649 ; 2041-2647
DOI	10.1093/bfgp/elv013
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Article: A Perspective on CRN Proteins in the Genomics Age: Evolution, Classification, Delivery and Function Revisited.

Amaro, Tiago M M M / Thilliez, Gaëtan J A / Motion, Graham B / Huitema, Edgar

Frontiers in plant science

2017 Volume 8, Page(s) 99

Abstract: Plant associated microbes rely on secreted virulence factors (effectors) to modulate host immunity and ensure progressive infection. Amongst the secreted protein repertoires defined and studied in pathogens to date, the CRNs (for CRinkling and Necrosis) ... ...

Abstract	Plant associated microbes rely on secreted virulence factors (effectors) to modulate host immunity and ensure progressive infection. Amongst the secreted protein repertoires defined and studied in pathogens to date, the CRNs (for CRinkling and Necrosis) have emerged as one of only a few highly conserved protein families, spread across several kingdoms. CRN proteins were first identified in plant pathogenic oomycetes where they were found to be modular factors that are secreted and translocated inside host cells by means of a conserved N-terminal domain. Subsequent localization and functional studies have led to the view that CRN C-termini execute their presumed effector function in the host nucleus, targeting processes required for immunity. These findings have led to great interest in this large protein family and driven the identification of additional CRN-like proteins in other organisms. The identification of CRN proteins and subsequent functional studies have markedly increased the number of candidate CRN protein sequences, expanded the range of phenotypes tentatively associated with function and revealed some of their molecular functions toward virulence. The increased number of characterized CRNs also has presented a set of challenges that may impede significant progress in the future. Here, we summarize our current understanding of the CRNs and re-assess some basic assumptions regarding this protein family. We will discuss the latest findings on CRN biology and highlight exciting new hypotheses that have emanated from the field. Finally, we will discuss new approaches to study CRN functions that would lead to a better understanding of CRN effector biology as well as the processes that lead to host susceptibility and immunity.
Language	English
Publishing date	2017-02-03
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2017.00099
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Article ; Online: Random mutagenesis screen shows that Phytophthora capsici CRN83_152-mediated cell death is not required for its virulence function(s).

Amaro, Tiago M M M / Thilliez, Gaëtan J A / Mcleod, Rory A / Huitema, Edgar

Molecular plant pathology

2017 Volume 19, Issue 5, Page(s) 1114–1126

Abstract: With the increasing availability of plant pathogen genomes, secreted proteins that aid infection (effectors) have emerged as key factors that help to govern plant-microbe interactions. The conserved CRN (CRinkling and Necrosis) effector family was first ... ...

Abstract	With the increasing availability of plant pathogen genomes, secreted proteins that aid infection (effectors) have emerged as key factors that help to govern plant-microbe interactions. The conserved CRN (CRinkling and Necrosis) effector family was first described in oomycetes by their capacity to induce host cell death. Despite recent advances towards the elucidation of CRN virulence functions, the relevance of CRN-induced cell death remains unclear. In planta over-expression of PcCRN83_152, a CRN effector from Phytophthora capsici, causes host cell death and boosts P. capsici virulence. We used these features to ask whether PcCRN83_152-induced cell death is linked to its virulence function. By randomly mutating this effector, we generated PcCRN83_152 variants with no cell death (NCD) phenotypes, which were subsequently tested for activity towards enhanced virulence. We showed that a subset of PcCRN83_152 NCD variants retained their ability to boost P. capsici virulence. Moreover, NCD variants were shown to have a suppressive effect on PcCRN83_152-mediated cell death. Our work shows that PcCRN83_152-induced cell death and virulence function can be separated. Moreover, if these findings hold true for other cell death-inducing CRN effectors, this work, in turn, will provide a framework for studies aimed at unveiling the virulence functions of these effectors.
MeSH term(s)	Amino Acid Sequence ; Base Sequence ; Cell Death ; Chromatin/metabolism ; Genetic Testing ; Mutagenesis/genetics ; Phenotype ; Phytophthora/genetics ; Phytophthora/pathogenicity ; Proteins/chemistry ; Proteins/genetics ; Nicotiana/cytology ; Nicotiana/microbiology ; Virulence
Chemical Substances	Chromatin ; Proteins
Language	English
Publishing date	2017-10-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2020755-4
ISSN	1364-3703 ; 1364-3703
ISSN (online)	1364-3703
ISSN	1364-3703
DOI	10.1111/mpp.12590
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