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Structure and evolution of barley powdery mildew effector candidates

BACKGROUND: Protein effectors of pathogenicity are instrumental in modulating host immunity and disease resistance. The powdery mildew pathogen of grasses Blumeria graminis causes one of the most important diseases of cereal crops. B. graminis is an obligate biotrophic pathogen and as such has an ab...

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Autores principales: Pedersen, Carsten, van Themaat, Emiel Ver Loren, McGuffin, Liam J, Abbott, James C, Burgis, Timothy A, Barton, Geraint, Bindschedler, Laurence V, Lu, Xunli, Maekawa, Takaki, Weßling, Ralf, Cramer, Rainer, Thordal-Christensen, Hans, Panstruga, Ralph, Spanu, Pietro D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3582587/
https://www.ncbi.nlm.nih.gov/pubmed/23231440
http://dx.doi.org/10.1186/1471-2164-13-694
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author Pedersen, Carsten
van Themaat, Emiel Ver Loren
McGuffin, Liam J
Abbott, James C
Burgis, Timothy A
Barton, Geraint
Bindschedler, Laurence V
Lu, Xunli
Maekawa, Takaki
Weßling, Ralf
Cramer, Rainer
Thordal-Christensen, Hans
Panstruga, Ralph
Spanu, Pietro D
author_facet Pedersen, Carsten
van Themaat, Emiel Ver Loren
McGuffin, Liam J
Abbott, James C
Burgis, Timothy A
Barton, Geraint
Bindschedler, Laurence V
Lu, Xunli
Maekawa, Takaki
Weßling, Ralf
Cramer, Rainer
Thordal-Christensen, Hans
Panstruga, Ralph
Spanu, Pietro D
author_sort Pedersen, Carsten
collection PubMed
description BACKGROUND: Protein effectors of pathogenicity are instrumental in modulating host immunity and disease resistance. The powdery mildew pathogen of grasses Blumeria graminis causes one of the most important diseases of cereal crops. B. graminis is an obligate biotrophic pathogen and as such has an absolute requirement to suppress or avoid host immunity if it is to survive and cause disease. RESULTS: Here we characterise a superfamily predicted to be the full complement of Candidates for Secreted Effector Proteins (CSEPs) in the fungal barley powdery mildew parasite B. graminis f.sp. hordei. The 491 genes encoding these proteins constitute over 7% of this pathogen’s annotated genes and most were grouped into 72 families of up to 59 members. They were predominantly expressed in the intracellular feeding structures called haustoria, and proteins specifically associated with the haustoria were identified by large-scale mass spectrometry-based proteomics. There are two major types of effector families: one comprises shorter proteins (100–150 amino acids), with a high relative expression level in the haustoria and evidence of extensive diversifying selection between paralogs; the second type consists of longer proteins (300–400 amino acids), with lower levels of differential expression and evidence of purifying selection between paralogs. An analysis of the predicted protein structures underscores their overall similarity to known fungal effectors, but also highlights unexpected structural affinities to ribonucleases throughout the entire effector super-family. Candidate effector genes belonging to the same family are loosely clustered in the genome and are associated with repetitive DNA derived from retro-transposons. CONCLUSIONS: We employed the full complement of genomic, transcriptomic and proteomic analyses as well as structural prediction methods to identify and characterize the members of the CSEPs superfamily in B. graminis f.sp. hordei. Based on relative intron position and the distribution of CSEPs with a ribonuclease-like domain in the phylogenetic tree we hypothesize that the associated genes originated from an ancestral gene, encoding a secreted ribonuclease, duplicated successively by repetitive DNA-driven processes and diversified during the evolution of the grass and cereal powdery mildew lineage.
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spelling pubmed-35825872013-02-27 Structure and evolution of barley powdery mildew effector candidates Pedersen, Carsten van Themaat, Emiel Ver Loren McGuffin, Liam J Abbott, James C Burgis, Timothy A Barton, Geraint Bindschedler, Laurence V Lu, Xunli Maekawa, Takaki Weßling, Ralf Cramer, Rainer Thordal-Christensen, Hans Panstruga, Ralph Spanu, Pietro D BMC Genomics Research Article BACKGROUND: Protein effectors of pathogenicity are instrumental in modulating host immunity and disease resistance. The powdery mildew pathogen of grasses Blumeria graminis causes one of the most important diseases of cereal crops. B. graminis is an obligate biotrophic pathogen and as such has an absolute requirement to suppress or avoid host immunity if it is to survive and cause disease. RESULTS: Here we characterise a superfamily predicted to be the full complement of Candidates for Secreted Effector Proteins (CSEPs) in the fungal barley powdery mildew parasite B. graminis f.sp. hordei. The 491 genes encoding these proteins constitute over 7% of this pathogen’s annotated genes and most were grouped into 72 families of up to 59 members. They were predominantly expressed in the intracellular feeding structures called haustoria, and proteins specifically associated with the haustoria were identified by large-scale mass spectrometry-based proteomics. There are two major types of effector families: one comprises shorter proteins (100–150 amino acids), with a high relative expression level in the haustoria and evidence of extensive diversifying selection between paralogs; the second type consists of longer proteins (300–400 amino acids), with lower levels of differential expression and evidence of purifying selection between paralogs. An analysis of the predicted protein structures underscores their overall similarity to known fungal effectors, but also highlights unexpected structural affinities to ribonucleases throughout the entire effector super-family. Candidate effector genes belonging to the same family are loosely clustered in the genome and are associated with repetitive DNA derived from retro-transposons. CONCLUSIONS: We employed the full complement of genomic, transcriptomic and proteomic analyses as well as structural prediction methods to identify and characterize the members of the CSEPs superfamily in B. graminis f.sp. hordei. Based on relative intron position and the distribution of CSEPs with a ribonuclease-like domain in the phylogenetic tree we hypothesize that the associated genes originated from an ancestral gene, encoding a secreted ribonuclease, duplicated successively by repetitive DNA-driven processes and diversified during the evolution of the grass and cereal powdery mildew lineage. BioMed Central 2012-12-11 /pmc/articles/PMC3582587/ /pubmed/23231440 http://dx.doi.org/10.1186/1471-2164-13-694 Text en Copyright ©2012 Pedersen et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Pedersen, Carsten
van Themaat, Emiel Ver Loren
McGuffin, Liam J
Abbott, James C
Burgis, Timothy A
Barton, Geraint
Bindschedler, Laurence V
Lu, Xunli
Maekawa, Takaki
Weßling, Ralf
Cramer, Rainer
Thordal-Christensen, Hans
Panstruga, Ralph
Spanu, Pietro D
Structure and evolution of barley powdery mildew effector candidates
title Structure and evolution of barley powdery mildew effector candidates
title_full Structure and evolution of barley powdery mildew effector candidates
title_fullStr Structure and evolution of barley powdery mildew effector candidates
title_full_unstemmed Structure and evolution of barley powdery mildew effector candidates
title_short Structure and evolution of barley powdery mildew effector candidates
title_sort structure and evolution of barley powdery mildew effector candidates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3582587/
https://www.ncbi.nlm.nih.gov/pubmed/23231440
http://dx.doi.org/10.1186/1471-2164-13-694
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