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Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae

BACKGROUND: Rice, which serves as a staple food for more than half of the world’s population, is very susceptible to the pathogenic fungus, Magnaporthe oryzae. However, common wild rice (Oryza rufipogon), which is the ancestor of Asian cultivated rice (O. sativa), has significant potential as a gene...

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Autores principales: Tian, Lei, Chang, Chunling, Ma, Lina, Nasir, Fahad, Zhang, Jianfeng, Li, Weiqiang, Tran, Lam-Son Phan, Tian, Chunjie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6510786/
https://www.ncbi.nlm.nih.gov/pubmed/31076886
http://dx.doi.org/10.1186/s12284-019-0287-9
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author Tian, Lei
Chang, Chunling
Ma, Lina
Nasir, Fahad
Zhang, Jianfeng
Li, Weiqiang
Tran, Lam-Son Phan
Tian, Chunjie
author_facet Tian, Lei
Chang, Chunling
Ma, Lina
Nasir, Fahad
Zhang, Jianfeng
Li, Weiqiang
Tran, Lam-Son Phan
Tian, Chunjie
author_sort Tian, Lei
collection PubMed
description BACKGROUND: Rice, which serves as a staple food for more than half of the world’s population, is very susceptible to the pathogenic fungus, Magnaporthe oryzae. However, common wild rice (Oryza rufipogon), which is the ancestor of Asian cultivated rice (O. sativa), has significant potential as a genetic source of resistance to M. oryzae. Recent studies have shown that the domestication of rice has altered its relationship to symbiotic arbuscular mycorrhizae. A comparative response of wild and domestic rice inhabited by mycorrhizae to infection by M. oryzae has not been documented. RESULTS: In the current study, roots of wild and cultivated rice colonized with the arbuscular mycorrhizal (AM) fungus (AMF) Rhizoglomus intraradices were used to compare the transcriptomic responses of the two species to infection by M. oryzae. Phenotypic analysis indicated that the colonization of wild and cultivated rice with R. intraradices improved the resistance of both genotypes to M. oryzae. Wild AM rice, however, was more resistant to M. oryzae than the cultivated AM rice, as well as nonmycorrhizal roots of wild rice. Transcriptome analysis indicated that the mechanisms regulating the responses of wild and cultivated AM rice to M. oryzae invasion were significantly different. The expression of a greater number of genes was changed in wild AM rice than in cultivated AM rice in response to the pathogen. Both wild and cultivated AM rice exhibited a shared response to M. oryzae which included genes related to the auxin and salicylic acid pathways; all of these play important roles in pathogenesis-related protein synthesis. In wild AM rice, secondary metabolic and biotic stress-related analyses indicated that the jasmonic acid synthesis-related α-linolenic acid pathway, the phenolic and terpenoid pathways, as well as the phenolic and terpenoid syntheses-related mevalonate (MVA) pathway were more affected by the pathogen. Genes related to these pathways were more significantly enriched in wild AM rice than in cultivated AM rice in response to M. oryzae. On the other hand, genes associated with the ‘brassinosteroid biosynthesis’ were more enriched in cultivated AM rice. CONCLUSIONS: The AMF R. intraradices-colonized rice plants exhibited greater resistance to M. oryzae than non-AMF-colonized plants. The findings of the current study demonstrate the potential effects of crop domestication on the benefits received by the host via root colonization with AMF(s), and provide new information on the underlying molecular mechanisms. In addition, results of this study can also help develop guidelines for the applications of AMF(s) when planting rice. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12284-019-0287-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-65107862019-05-28 Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae Tian, Lei Chang, Chunling Ma, Lina Nasir, Fahad Zhang, Jianfeng Li, Weiqiang Tran, Lam-Son Phan Tian, Chunjie Rice (N Y) Original Article BACKGROUND: Rice, which serves as a staple food for more than half of the world’s population, is very susceptible to the pathogenic fungus, Magnaporthe oryzae. However, common wild rice (Oryza rufipogon), which is the ancestor of Asian cultivated rice (O. sativa), has significant potential as a genetic source of resistance to M. oryzae. Recent studies have shown that the domestication of rice has altered its relationship to symbiotic arbuscular mycorrhizae. A comparative response of wild and domestic rice inhabited by mycorrhizae to infection by M. oryzae has not been documented. RESULTS: In the current study, roots of wild and cultivated rice colonized with the arbuscular mycorrhizal (AM) fungus (AMF) Rhizoglomus intraradices were used to compare the transcriptomic responses of the two species to infection by M. oryzae. Phenotypic analysis indicated that the colonization of wild and cultivated rice with R. intraradices improved the resistance of both genotypes to M. oryzae. Wild AM rice, however, was more resistant to M. oryzae than the cultivated AM rice, as well as nonmycorrhizal roots of wild rice. Transcriptome analysis indicated that the mechanisms regulating the responses of wild and cultivated AM rice to M. oryzae invasion were significantly different. The expression of a greater number of genes was changed in wild AM rice than in cultivated AM rice in response to the pathogen. Both wild and cultivated AM rice exhibited a shared response to M. oryzae which included genes related to the auxin and salicylic acid pathways; all of these play important roles in pathogenesis-related protein synthesis. In wild AM rice, secondary metabolic and biotic stress-related analyses indicated that the jasmonic acid synthesis-related α-linolenic acid pathway, the phenolic and terpenoid pathways, as well as the phenolic and terpenoid syntheses-related mevalonate (MVA) pathway were more affected by the pathogen. Genes related to these pathways were more significantly enriched in wild AM rice than in cultivated AM rice in response to M. oryzae. On the other hand, genes associated with the ‘brassinosteroid biosynthesis’ were more enriched in cultivated AM rice. CONCLUSIONS: The AMF R. intraradices-colonized rice plants exhibited greater resistance to M. oryzae than non-AMF-colonized plants. The findings of the current study demonstrate the potential effects of crop domestication on the benefits received by the host via root colonization with AMF(s), and provide new information on the underlying molecular mechanisms. In addition, results of this study can also help develop guidelines for the applications of AMF(s) when planting rice. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12284-019-0287-9) contains supplementary material, which is available to authorized users. Springer US 2019-05-10 /pmc/articles/PMC6510786/ /pubmed/31076886 http://dx.doi.org/10.1186/s12284-019-0287-9 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.
spellingShingle Original Article
Tian, Lei
Chang, Chunling
Ma, Lina
Nasir, Fahad
Zhang, Jianfeng
Li, Weiqiang
Tran, Lam-Son Phan
Tian, Chunjie
Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title_full Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title_fullStr Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title_full_unstemmed Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title_short Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae
title_sort comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen magnaporthe oryzae
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6510786/
https://www.ncbi.nlm.nih.gov/pubmed/31076886
http://dx.doi.org/10.1186/s12284-019-0287-9
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