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Article: Differential Expression of Candidate Salivary Effector Genes in Pea Aphid Biotypes With Distinct Host Plant Specificity.

Boulain, Hélène / Legeai, Fabrice / Jaquiéry, Julie / Guy, Endrick / Morlière, Stéphanie / Simon, Jean-Christophe / Sugio, Akiko

Frontiers in plant science

2019 Volume 10, Page(s) 1301

Abstract: Effector proteins play crucial roles in determining the outcome of various plant-parasite interactions. Aphids inject salivary effector proteins into plants to facilitate phloem feeding, but some proteins might trigger defense responses in certain plants. ...

Abstract	Effector proteins play crucial roles in determining the outcome of various plant-parasite interactions. Aphids inject salivary effector proteins into plants to facilitate phloem feeding, but some proteins might trigger defense responses in certain plants. The pea aphid,
Language	English
Publishing date	2019-10-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2711035-7
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2019.01301
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Big Genes, Small Effectors: Pea Aphid Cassette Effector Families Composed From Miniature Exons.

Dommel, Matthew / Oh, Jonghee / Huguet-Tapia, Jose Carlos / Guy, Endrick / Boulain, Hélène / Sugio, Akiko / Murugan, Marimuthu / Legeai, Fabrice / Heck, Michelle / Smith, C Michael / White, Frank F

Frontiers in plant science

2020 Volume 11, Page(s) 1230

Abstract: Aphids secrete proteins from their stylets that evidence indicates function similar to pathogen effectors for virulence. Here, we describe two small candidate effector gene families of the pea aphid, ...

Abstract	Aphids secrete proteins from their stylets that evidence indicates function similar to pathogen effectors for virulence. Here, we describe two small candidate effector gene families of the pea aphid,
Language	English
Publishing date	2020-09-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2711035-7
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2020.01230
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Genome Sequence of Xanthomonas campestris pv. campestris Strain Xca5

Bolot, Stéphanie / Guy, Endrick / Carrere, Sébastien / Barbe, Valérie / Arlat, Matthieu / Noël, Laurent D

Genome announcements. 2013 Feb. 28, v. 1, no. 1

2013

Abstract: An annotated high-quality draft genome sequence for Xanthomonas campestris pv. campestris race 1 strain Xca5 (originally described as X. campestris pv. armoraciae), the causal agent of black rot on Brassicaceae plants, has been determined. This genome ... ...

Abstract	An annotated high-quality draft genome sequence for Xanthomonas campestris pv. campestris race 1 strain Xca5 (originally described as X. campestris pv. armoraciae), the causal agent of black rot on Brassicaceae plants, has been determined. This genome sequence is a valuable resource for comparative genomics within the campestris pathovar.
Keywords	Brassicaceae ; Xanthomonas campestris pv. campestris ; genome ; genomics ; nucleotide sequences ; pathovars
Language	English
Dates of publication	2013-0228
Size	p. e00032-12.
Publishing place	American Society for Microbiology
Document type	Article
ZDB-ID	2704277-7
ISSN	2169-8287
ISSN	2169-8287
DOI	10.1128/genomeA.00032-12
Database	NAL-Catalogue (AGRICOLA)

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Article: Genome Sequence of Xanthomonas campestris pv. campestris Strain Xca5.

Bolot, Stéphanie / Guy, Endrick / Carrere, Sébastien / Barbe, Valérie / Arlat, Matthieu / Noël, Laurent D

Genome announcements

2013 Volume 1, Issue 1

Abstract	An annotated high-quality draft genome sequence for Xanthomonas campestris pv. campestris race 1 strain Xca5 (originally described as X. campestris pv. armoraciae), the causal agent of black rot on Brassicaceae plants, has been determined. This genome sequence is a valuable resource for comparative genomics within the campestris pathovar.
Language	English
Publishing date	2013-02-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	2704277-7
ISSN	2169-8287
ISSN	2169-8287
DOI	10.1128/genomeA.00032-12
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Fast Evolution and Lineage-Specific Gene Family Expansions of Aphid Salivary Effectors Driven by Interactions with Host-Plants.

Boulain, Hélène / Legeai, Fabrice / Guy, Endrick / Morlière, Stéphanie / Douglas, Nadine E / Oh, Jonghee / Murugan, Marimuthu / Smith, Michael / Jaquiéry, Julie / Peccoud, Jean / White, Frank F / Carolan, James C / Simon, Jean-Christophe / Sugio, Akiko

Genome biology and evolution

2018 Volume 10, Issue 6, Page(s) 1554–1572

Abstract: Effector proteins play crucial roles in plant-parasite interactions by suppressing plant defenses and hijacking plant physiological responses to facilitate parasite invasion and propagation. Although effector proteins have been characterized in many ... ...

Abstract	Effector proteins play crucial roles in plant-parasite interactions by suppressing plant defenses and hijacking plant physiological responses to facilitate parasite invasion and propagation. Although effector proteins have been characterized in many microbial plant pathogens, their nature and role in adaptation to host plants are largely unknown in insect herbivores. Aphids rely on salivary effector proteins injected into the host plants to promote phloem sap uptake. Therefore, gaining insight into the repertoire and evolution of aphid effectors is key to unveiling the mechanisms responsible for aphid virulence and host plant specialization. With this aim in mind, we assembled catalogues of putative effectors in the legume specialist aphid, Acyrthosiphon pisum, using transcriptomics and proteomics approaches. We identified 3,603 candidate effector genes predicted to be expressed in A. pisum salivary glands (SGs), and 740 of which displayed up-regulated expression in SGs in comparison to the alimentary tract. A search for orthologs in 17 arthropod genomes revealed that SG-up-regulated effector candidates of A. pisum are enriched in aphid-specific genes and tend to evolve faster compared with the whole gene set. We also found that a large fraction of proteins detected in the A. pisum saliva belonged to three gene families, of which certain members show evidence consistent with positive selection. Overall, this comprehensive analysis suggests that the large repertoire of effector candidates in A. pisum constitutes a source of novelties promoting plant adaptation to legumes.
MeSH term(s)	Adaptation, Biological/genetics ; Animals ; Aphids/genetics ; Evolution, Molecular ; Host-Pathogen Interactions/genetics ; Insect Proteins/genetics ; Plants/parasitology ; Proteomics/methods ; Salivary Proteins and Peptides/genetics ; Transcriptome/genetics ; Up-Regulation/genetics ; Virulence/genetics
Chemical Substances	Insect Proteins ; Salivary Proteins and Peptides
Language	English
Publishing date	2018-05-22
Publishing country	England
Document type	Comparative Study ; Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1759-6653
ISSN (online)	1759-6653
DOI	10.1093/gbe/evy097
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Two ancestral genes shaped the Xanthomonas campestris TAL effector gene repertoire.

Denancé, Nicolas / Szurek, Boris / Doyle, Erin L / Lauber, Emmanuelle / Fontaine-Bodin, Lisa / Carrère, Sébastien / Guy, Endrick / Hajri, Ahmed / Cerutti, Aude / Boureau, Tristan / Poussier, Stéphane / Arlat, Matthieu / Bogdanove, Adam J / Noël, Laurent D

The New phytologist

2018 Volume 219, Issue 1, Page(s) 391–407

Abstract: Xanthomonas transcription activator-like effectors (TALEs) are injected inside plant cells to promote host susceptibility by enhancing transcription of host susceptibility genes. TALE-encoding (tal) genes were thought to be absent from Brassicaceae- ... ...

Abstract	Xanthomonas transcription activator-like effectors (TALEs) are injected inside plant cells to promote host susceptibility by enhancing transcription of host susceptibility genes. TALE-encoding (tal) genes were thought to be absent from Brassicaceae-infecting Xanthomonas campestris (Xc) genomes based on four reference genomic sequences. We discovered tal genes in 26 of 49 Xc strains isolated worldwide and used a combination of single molecule real time (SMRT) and tal amplicon sequencing to yield a near-complete description of the TALEs found in Xc (Xc TALome). The 53 sequenced tal genes encode 21 distinct DNA binding domains that sort into seven major DNA binding specificities. In silico analysis of the Brassica rapa promoterome identified a repertoire of predicted TALE targets, five of which were experimentally validated using quantitative reverse transcription polymerase chain reaction. The Xc TALome shows multiple signs of DNA rearrangements that probably drove its evolution from two ancestral tal genes. We discovered that Tal12a and Tal15a of Xcc strain Xca5 contribute together in the development of disease symptoms on susceptible B. oleracea var. botrytis cv Clovis. This large and polymorphic repertoire of TALEs opens novel perspectives for elucidating TALE-mediated susceptibility of Brassicaceae to black rot disease and for understanding the molecular processes underlying TALE evolution.
MeSH term(s)	Brassica/microbiology ; Genome, Bacterial ; Host-Pathogen Interactions/genetics ; Phylogeny ; Plant Diseases/microbiology ; Transcription Activator-Like Effectors/genetics ; Xanthomonas campestris/genetics ; Xanthomonas campestris/pathogenicity
Chemical Substances	Transcription Activator-Like Effectors
Language	English
Publishing date	2018-04-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.15148
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Corrigendum: Optimization of Agroinfiltration in

Guy, Endrick / Boulain, Hélène / Aigu, Yoann / Le Pennec, Charlotte / Chawki, Khaoula / Morlière, Stéphanie / Schädel, Kristina / Kunert, Grit / Simon, Jean-Christophe / Sugio, Akiko

Frontiers in plant science

2017 Volume 7, Page(s) 2046

Abstract: This corrects the article on p. 1171 in vol. 7, PMID: 27555856.]. ...

Abstract	[This corrects the article on p. 1171 in vol. 7, PMID: 27555856.].
Language	English
Publishing date	2017-01-10
Publishing country	Switzerland
Document type	Published Erratum
ZDB-ID	2711035-7
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2016.02046
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK.

Guy, Endrick / Lautier, Martine / Chabannes, Matthieu / Roux, Brice / Lauber, Emmanuelle / Arlat, Matthieu / Noël, Laurent D

PloS one

2013 Volume 8, Issue 8, Page(s) e73469

Abstract: Xanthomonas campestris pv. campestris (Xcc) colonizes the vascular system of Brassicaceae and ultimately causes black rot. In susceptible Arabidopsis plants, XopAC type III effector inhibits by uridylylation positive regulators of the PAMP-triggered ... ...

Abstract	Xanthomonas campestris pv. campestris (Xcc) colonizes the vascular system of Brassicaceae and ultimately causes black rot. In susceptible Arabidopsis plants, XopAC type III effector inhibits by uridylylation positive regulators of the PAMP-triggered immunity such as the receptor-like cytoplasmic kinases (RLCK) BIK1 and PBL1. In the resistant ecotype Col-0, xopAC is a major avirulence gene of Xcc. In this study, we show that both the RLCK interaction domain and the uridylyl transferase domain of XopAC are required for avirulence. Furthermore, xopAC can also confer avirulence to both the vascular pathogen Ralstonia solanacearum and the mesophyll-colonizing pathogen Pseudomonas syringae indicating that xopAC-specified effector-triggered immunity is not specific to the vascular system. In planta, XopAC-YFP fusions are localized at the plasma membrane suggesting that XopAC might interact with membrane-localized proteins. Eight RLCK of subfamily VII predicted to be localized at the plasma membrane and interacting with XopAC in yeast two-hybrid assays have been isolated. Within this subfamily, PBL2 and RIPK RLCK genes but not BIK1 are important for xopAC-specified effector-triggered immunity and Arabidopsis resistance to Xcc.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/immunology ; Arabidopsis/microbiology ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Bacterial Proteins/genetics ; Cell Membrane/enzymology ; Cell Membrane/genetics ; Cytoplasm/enzymology ; Cytoplasm/genetics ; Gene Expression Regulation, Plant ; Genes, Reporter ; Host-Pathogen Interactions ; Luminescent Proteins/genetics ; Plant Cells/metabolism ; Plant Cells/microbiology ; Plant Diseases/genetics ; Plant Diseases/immunology ; Plant Diseases/microbiology ; Plant Immunity/genetics ; Protein Kinases/genetics ; Protein Kinases/metabolism ; Protein-Serine-Threonine Kinases/genetics ; Protein-Serine-Threonine Kinases/metabolism ; Pseudomonas syringae/physiology ; Ralstonia solanacearum/physiology ; Xanthomonas campestris/physiology
Chemical Substances	Arabidopsis Proteins ; Bacterial Proteins ; Luminescent Proteins ; yellow fluorescent protein, Bacteria ; Protein Kinases (EC 2.7.-) ; RPM1-induced protein kinase, Arabidopsis (EC 2.7.-) ; Protein-Serine-Threonine Kinases (EC 2.7.11.1) ; receptor-like protein kinase 2, Arabidopsis (EC 2.7.11.1)
Language	English
Publishing date	2013-08-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0073469
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Optimization of Agroinfiltration in Pisum sativum Provides a New Tool for Studying the Salivary Protein Functions in the Pea Aphid Complex.

Guy, Endrick / Boulain, Hélène / Aigu, Yoann / Le Pennec, Charlotte / Chawki, Khaoula / Morlière, Stéphanie / Schädel, Kristina / Kunert, Grit / Simon, Jean-Christophe / Sugio, Akiko

Frontiers in plant science

2016 Volume 7, Page(s) 1171

Abstract: Aphids are piercing-sucking insect pests and feed on phloem sap. During feeding, aphids inject a battery of salivary proteins into host plant. Some of these proteins function like effectors of microbial pathogens and influence the outcome of plant-aphid ... ...

Abstract	Aphids are piercing-sucking insect pests and feed on phloem sap. During feeding, aphids inject a battery of salivary proteins into host plant. Some of these proteins function like effectors of microbial pathogens and influence the outcome of plant-aphid interactions. The pea aphid (Acyrthosiphon pisum) is the model aphid and encompasses multiple biotypes each specialized to one or a few legume species, providing an opportunity to investigate the underlying mechanisms of the compatibility between plants and aphid biotypes. We aim to identify the aphid factors that determine the compatibility with host plants, hence involved in the host plant specialization process, and hypothesize that salivary proteins are one of those factors. Agrobacterium-mediated transient gene expression is a powerful tool to perform functional analyses of effector (salivary) proteins in plants. However, the tool was not established for the legume species that A. pisum feeds on. Thus, we decided to optimize the method for legume plants to facilitate the functional analyses of A. pisum salivary proteins. We screened a range of cultivars of pea (Pisum sativum) and alfalfa (Medicago sativa). None of the M. sativa cultivars was suitable for agroinfiltration under the tested conditions; however, we established a protocol for efficient transient gene expression in two cultivars of P. sativum, ZP1109 and ZP1130, using A. tumefaciens AGL-1 strain and the pEAQ-HT-DEST1 vector. We confirmed that the genes are expressed from 3 to 10 days post-infiltration and that aphid lines of the pea adapted biotype fed and reproduced on these two cultivars while lines of alfalfa and clover biotypes did not. Thus, the pea biotype recognizes these two cultivars as typical pea plants. By using a combination of ZP1109 and an A. pisum line, we defined an agroinfiltration procedure to examine the effect of in planta expression of selected salivary proteins on A. pisum fitness and demonstrated that transient expression of one candidate salivary gene increased the fecundity of the aphids. This result confirms that the agroinfiltration can be used to perform functional analyses of salivary proteins in P. sativum and consequently to study the molecular mechanisms underlying host specialization in the pea aphid complex.
Language	English
Publishing date	2016-08-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2711035-7
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2016.01171
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Article: Natural Genetic Variation of Xanthomonas campestris pv. campestris Pathogenicity on Arabidopsis Revealed by Association and Reverse Genetics

Guy, Endrick / Genissel, Anne / Hajri, Ahmed / Chabannes, Matthieu / David, Perrine / Carrere, Sébastien / Lautier, Martine / Roux, Brice / Boureau, Tristan / Arlat, Matthieu / Poussier, Stéphane / Noël, Laurent D

mBio. 2013 July 1, v. 4, no. 3

2013

Abstract: The pathogenic bacterium Xanthomonas campestris pv. campestris, the causal agent of black rot of Brassicaceae, manipulates the physiology and the innate immunity of its hosts. Association genetic and reverse-genetic analyses of a world panel of 45 X. ... ...

Abstract	The pathogenic bacterium Xanthomonas campestris pv. campestris, the causal agent of black rot of Brassicaceae, manipulates the physiology and the innate immunity of its hosts. Association genetic and reverse-genetic analyses of a world panel of 45 X. campestris pv. campestris strains were used to gain understanding of the genetic basis of the bacterium’s pathogenicity to Arabidopsis thaliana . We found that the compositions of the minimal predicted type III secretome varied extensively, with 18 to 28 proteins per strain. There were clear differences in aggressiveness of those X. campestris pv. campestris strains on two Arabidopsis natural accessions. We identified 3 effector genes (xopAC , xopJ5 , and xopAL2) and 67 amplified fragment length polymorphism (AFLP) markers that were associated with variations in disease symptoms. The nature and distribution of the AFLP markers remain to be determined, but we observed a low linkage disequilibrium level between predicted effectors and other significant markers, suggesting that additional genetic factors make a meaningful contribution to pathogenicity. Mutagenesis of type III effectors in X. campestris pv. campestris confirmed that xopAC functions as both a virulence and an avirulence gene in Arabidopsis and that xopAM functions as a second avirulence gene on plants of the Col-0 ecotype. However, we did not detect the effect of any other effector in the X. campestris pv. campestris 8004 strain, likely due to other genetic background effects. These results highlight the complex genetic basis of pathogenicity at the pathovar level and encourage us to challenge the agronomical relevance of some virulence determinants identified solely in model strains. IMPORTANCE The identification and understanding of the genetic determinants of bacterial virulence are essential to be able to design efficient protection strategies for infected plants. The recent availability of genomic resources for a limited number of pathogen isolates and host genotypes has strongly biased our research toward genotype-specific approaches. Indeed, these do not consider the natural variation in both pathogens and hosts, so their applied relevance should be challenged. In our study, we exploited the genetic diversity of Xanthomonas campestris pv. campestris, the causal agent of black rot on Brassicaceae (e.g., cabbage), to mine for pathogenicity determinants. This work evidenced the contribution of known and unknown loci to pathogenicity relevant at the pathovar level and identified these virulence determinants as prime targets for breeding resistance to X. campestris pv. campestris in Brassicaceae.
Keywords	Arabidopsis thaliana ; Xanthomonas campestris pv. campestris ; amplified fragment length polymorphism ; bacteria ; bacterial diseases of plants ; bacterial proteins ; breeding ; cabbage ; ecotypes ; genes ; genetic background ; genetic markers ; genetic variation ; hosts ; linkage disequilibrium ; loci ; mutagenesis ; pathogens ; pathovars ; virulence
Language	English
Dates of publication	2013-0701
Size	p. e00538-12.
Publishing place	American Society for Microbiology
Document type	Article
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00538-12
Database	NAL-Catalogue (AGRICOLA)

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