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Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance
BACKGROUND: The large and highly repetitive genomes of the cultivated species Hordeum vulgare (barley), Triticum aestivum (wheat), and Secale cereale (rye) belonging to the Triticeae tribe of grasses appear to be particularly rich in gene-like sequences including partial duplicates. Most of them hav...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092874/ https://www.ncbi.nlm.nih.gov/pubmed/30111359 http://dx.doi.org/10.1186/s13059-018-1472-7 |
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author | Rajaraman, Jeyaraman Douchkov, Dimitar Lück, Stefanie Hensel, Götz Nowara, Daniela Pogoda, Maria Rutten, Twan Meitzel, Tobias Brassac, Jonathan Höfle, Caroline Hückelhoven, Ralph Klinkenberg, Jörn Trujillo, Marco Bauer, Eva Schmutzer, Thomas Himmelbach, Axel Mascher, Martin Lazzari, Barbara Stein, Nils Kumlehn, Jochen Schweizer, Patrick |
author_facet | Rajaraman, Jeyaraman Douchkov, Dimitar Lück, Stefanie Hensel, Götz Nowara, Daniela Pogoda, Maria Rutten, Twan Meitzel, Tobias Brassac, Jonathan Höfle, Caroline Hückelhoven, Ralph Klinkenberg, Jörn Trujillo, Marco Bauer, Eva Schmutzer, Thomas Himmelbach, Axel Mascher, Martin Lazzari, Barbara Stein, Nils Kumlehn, Jochen Schweizer, Patrick |
author_sort | Rajaraman, Jeyaraman |
collection | PubMed |
description | BACKGROUND: The large and highly repetitive genomes of the cultivated species Hordeum vulgare (barley), Triticum aestivum (wheat), and Secale cereale (rye) belonging to the Triticeae tribe of grasses appear to be particularly rich in gene-like sequences including partial duplicates. Most of them have been classified as putative pseudogenes. In this study we employ transient and stable gene silencing- and over-expression systems in barley to study the function of HvARM1 (for H. vulgare Armadillo 1), a partial gene duplicate of the U-box/armadillo-repeat E3 ligase HvPUB15 (for H. vulgare Plant U-Box 15). RESULTS: The partial ARM1 gene is derived from a gene-duplication event in a common ancestor of the Triticeae and contributes to quantitative host as well as nonhost resistance to the biotrophic powdery mildew fungus Blumeria graminis. In barley, allelic variants of HvARM1 but not of HvPUB15 are significantly associated with levels of powdery mildew infection. Both HvPUB15 and HvARM1 proteins interact in yeast and plant cells with the susceptibility-related, plastid-localized barley homologs of THF1 (for Thylakoid formation 1) and of ClpS1 (for Clp-protease adaptor S1) of Arabidopsis thaliana. A genome-wide scan for partial gene duplicates reveals further events in barley resulting in stress-regulated, potentially neo-functionalized, genes. CONCLUSION: The results suggest neo-functionalization of the partial gene copy HvARM1 increases resistance against powdery mildew infection. It further links plastid function with susceptibility to biotrophic pathogen attack. These findings shed new light on a novel mechanism to employ partial duplication of protein-protein interaction domains to facilitate the expansion of immune signaling networks. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-018-1472-7) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6092874 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-60928742018-08-20 Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance Rajaraman, Jeyaraman Douchkov, Dimitar Lück, Stefanie Hensel, Götz Nowara, Daniela Pogoda, Maria Rutten, Twan Meitzel, Tobias Brassac, Jonathan Höfle, Caroline Hückelhoven, Ralph Klinkenberg, Jörn Trujillo, Marco Bauer, Eva Schmutzer, Thomas Himmelbach, Axel Mascher, Martin Lazzari, Barbara Stein, Nils Kumlehn, Jochen Schweizer, Patrick Genome Biol Research BACKGROUND: The large and highly repetitive genomes of the cultivated species Hordeum vulgare (barley), Triticum aestivum (wheat), and Secale cereale (rye) belonging to the Triticeae tribe of grasses appear to be particularly rich in gene-like sequences including partial duplicates. Most of them have been classified as putative pseudogenes. In this study we employ transient and stable gene silencing- and over-expression systems in barley to study the function of HvARM1 (for H. vulgare Armadillo 1), a partial gene duplicate of the U-box/armadillo-repeat E3 ligase HvPUB15 (for H. vulgare Plant U-Box 15). RESULTS: The partial ARM1 gene is derived from a gene-duplication event in a common ancestor of the Triticeae and contributes to quantitative host as well as nonhost resistance to the biotrophic powdery mildew fungus Blumeria graminis. In barley, allelic variants of HvARM1 but not of HvPUB15 are significantly associated with levels of powdery mildew infection. Both HvPUB15 and HvARM1 proteins interact in yeast and plant cells with the susceptibility-related, plastid-localized barley homologs of THF1 (for Thylakoid formation 1) and of ClpS1 (for Clp-protease adaptor S1) of Arabidopsis thaliana. A genome-wide scan for partial gene duplicates reveals further events in barley resulting in stress-regulated, potentially neo-functionalized, genes. CONCLUSION: The results suggest neo-functionalization of the partial gene copy HvARM1 increases resistance against powdery mildew infection. It further links plastid function with susceptibility to biotrophic pathogen attack. These findings shed new light on a novel mechanism to employ partial duplication of protein-protein interaction domains to facilitate the expansion of immune signaling networks. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-018-1472-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-15 /pmc/articles/PMC6092874/ /pubmed/30111359 http://dx.doi.org/10.1186/s13059-018-1472-7 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Rajaraman, Jeyaraman Douchkov, Dimitar Lück, Stefanie Hensel, Götz Nowara, Daniela Pogoda, Maria Rutten, Twan Meitzel, Tobias Brassac, Jonathan Höfle, Caroline Hückelhoven, Ralph Klinkenberg, Jörn Trujillo, Marco Bauer, Eva Schmutzer, Thomas Himmelbach, Axel Mascher, Martin Lazzari, Barbara Stein, Nils Kumlehn, Jochen Schweizer, Patrick Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title | Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title_full | Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title_fullStr | Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title_full_unstemmed | Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title_short | Evolutionarily conserved partial gene duplication in the Triticeae tribe of grasses confers pathogen resistance |
title_sort | evolutionarily conserved partial gene duplication in the triticeae tribe of grasses confers pathogen resistance |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092874/ https://www.ncbi.nlm.nih.gov/pubmed/30111359 http://dx.doi.org/10.1186/s13059-018-1472-7 |
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