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Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida

BACKGROUND: Tilletia horrida is a basidiomycete fungus that causes rice kernel smut, one of the most important rice diseases in hybrid rice growing areas worldwide. However, little is known about its mechanisms of pathogenicity. We previously reported the genome of T. horrida, and 597 genes that enc...

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Autores principales: Wang, Aijun, Pan, Linxiu, Niu, Xianyu, Shu, Xinyue, Yi, Xiaoqun, Yamamoto, Naoki, Li, Shuangcheng, Deng, Qiming, Zhu, Jun, Liang, Yueyang, Wang, Lingxia, Li, Ping, Zheng, Aiping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697988/
https://www.ncbi.nlm.nih.gov/pubmed/31419944
http://dx.doi.org/10.1186/s12870-019-1924-6
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author Wang, Aijun
Pan, Linxiu
Niu, Xianyu
Shu, Xinyue
Yi, Xiaoqun
Yamamoto, Naoki
Li, Shuangcheng
Deng, Qiming
Zhu, Jun
Liang, Yueyang
Wang, Lingxia
Li, Ping
Zheng, Aiping
author_facet Wang, Aijun
Pan, Linxiu
Niu, Xianyu
Shu, Xinyue
Yi, Xiaoqun
Yamamoto, Naoki
Li, Shuangcheng
Deng, Qiming
Zhu, Jun
Liang, Yueyang
Wang, Lingxia
Li, Ping
Zheng, Aiping
author_sort Wang, Aijun
collection PubMed
description BACKGROUND: Tilletia horrida is a basidiomycete fungus that causes rice kernel smut, one of the most important rice diseases in hybrid rice growing areas worldwide. However, little is known about its mechanisms of pathogenicity. We previously reported the genome of T. horrida, and 597 genes that encoded secreted proteins were annotated. Among these were some important effector genes related to pathogenicity. RESULTS: A secretome analysis suggested that five Tilletia fungi shared more gene families than were found in other smuts, and there was high conservation between them. Furthermore, we screened 597 secreted proteins from the T. horrida genome, some of which induced expression in host-pathogen interaction processes. Through transient expression, we demonstrated that two putative effectors could induce necrosis phenotypes in Nicotiana benthamiana. These two encoded genes were up-regulated during early infection, and the encoded proteins were confirmed to be secreted using a yeast secretion system. For the putative effector gene smut_5844, a signal peptide was required to induce non-host cell death, whereas ribonuclease catalytic active sites were required for smut_2965. Moreover, both putative effectors could induce an immune response in N. benthamiana leaves. Interestingly, one of the identified potential host interactors of smut_5844 was laccase-10 protein (OsLAC10), which has been predicted to be involved in plant lignification and iron metabolism. CONCLUSIONS: Overall, this study identified two secreted proteins in T. horrida that induce cell death or are involved in defense machinery in non-host plants. This research provides a useful foundation for understanding the interaction between rice and T. horrida. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1924-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-66979882019-08-19 Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida Wang, Aijun Pan, Linxiu Niu, Xianyu Shu, Xinyue Yi, Xiaoqun Yamamoto, Naoki Li, Shuangcheng Deng, Qiming Zhu, Jun Liang, Yueyang Wang, Lingxia Li, Ping Zheng, Aiping BMC Plant Biol Research Article BACKGROUND: Tilletia horrida is a basidiomycete fungus that causes rice kernel smut, one of the most important rice diseases in hybrid rice growing areas worldwide. However, little is known about its mechanisms of pathogenicity. We previously reported the genome of T. horrida, and 597 genes that encoded secreted proteins were annotated. Among these were some important effector genes related to pathogenicity. RESULTS: A secretome analysis suggested that five Tilletia fungi shared more gene families than were found in other smuts, and there was high conservation between them. Furthermore, we screened 597 secreted proteins from the T. horrida genome, some of which induced expression in host-pathogen interaction processes. Through transient expression, we demonstrated that two putative effectors could induce necrosis phenotypes in Nicotiana benthamiana. These two encoded genes were up-regulated during early infection, and the encoded proteins were confirmed to be secreted using a yeast secretion system. For the putative effector gene smut_5844, a signal peptide was required to induce non-host cell death, whereas ribonuclease catalytic active sites were required for smut_2965. Moreover, both putative effectors could induce an immune response in N. benthamiana leaves. Interestingly, one of the identified potential host interactors of smut_5844 was laccase-10 protein (OsLAC10), which has been predicted to be involved in plant lignification and iron metabolism. CONCLUSIONS: Overall, this study identified two secreted proteins in T. horrida that induce cell death or are involved in defense machinery in non-host plants. This research provides a useful foundation for understanding the interaction between rice and T. horrida. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1924-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-08-16 /pmc/articles/PMC6697988/ /pubmed/31419944 http://dx.doi.org/10.1186/s12870-019-1924-6 Text en © The Author(s). 2019 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 Article
Wang, Aijun
Pan, Linxiu
Niu, Xianyu
Shu, Xinyue
Yi, Xiaoqun
Yamamoto, Naoki
Li, Shuangcheng
Deng, Qiming
Zhu, Jun
Liang, Yueyang
Wang, Lingxia
Li, Ping
Zheng, Aiping
Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title_full Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title_fullStr Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title_full_unstemmed Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title_short Comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from Tilletia horrida
title_sort comparative secretome analysis of different smut fungi and identification of plant cell death-inducing secreted proteins from tilletia horrida
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697988/
https://www.ncbi.nlm.nih.gov/pubmed/31419944
http://dx.doi.org/10.1186/s12870-019-1924-6
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