Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>

ABSTRACT The blast fungus initiates infection using a heavily melanized, dome-shaped infection structure known as the appressorium, which forcibly ruptures the cuticle to enter the rice leaf tissue. How this process takes place remains not fully understood. Here, we used untargeted metabolomics anal...

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Autores principales:	Xiao-Hong Liu, Shuang Liang, Yun-Yun Wei, Xue-Ming Zhu, Lin Li, Ping-Ping Liu, Qing-Xia Zheng, Hui-Na Zhou, Yong Zhang, Li-Juan Mao, Caroline Mota Fernandes, Maurizio Del Poeta, Naweed I. Naqvi, Fu-Cheng Lin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	appressorium development early sphingolipid signaling inducer metabolomics analysis pathogenicity rice blast fungus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c3495fadcb6345b39a5b88071cf52395
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spelling	oai:doaj.org-article:c3495fadcb6345b39a5b88071cf523952021-11-15T16:22:09ZMetabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>10.1128/mBio.01467-192150-7511https://doaj.org/article/c3495fadcb6345b39a5b88071cf523952019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01467-19https://doaj.org/toc/2150-7511ABSTRACT The blast fungus initiates infection using a heavily melanized, dome-shaped infection structure known as the appressorium, which forcibly ruptures the cuticle to enter the rice leaf tissue. How this process takes place remains not fully understood. Here, we used untargeted metabolomics analyses to profile the metabolome of developing appressoria and identified significant changes in six key metabolic pathways, including early sphingolipid biosynthesis. Analyses employing small molecule inhibitors, gene disruption, or genetic and chemical complementation demonstrated that ceramide compounds of the sphingolipid biosynthesis pathway are essential for normal appressorial development controlled by mitosis. In addition, ceramide was found to act upstream from the protein kinase C-mediated cell wall integrity pathway during appressorium repolarization and pathogenicity in rice blast. Further discovery of the sphingolipid biosynthesis pathway revealed that glucosylceramide (GlcCer) synthesized by ceramide is the key substance affecting the pathogenicity of Magnaporthe oryzae. Our results provide new insights into the chemical moieties involved in the infection-related signaling networks, thereby revealing a potential target for the development of novel control agents against the major disease of rice and other cereals. IMPORTANCE Our untargeted analysis of metabolomics throughout the course of pathogenic development gave us an unprecedented high-resolution view of major shifts in metabolism that occur in the topmost fungal pathogen that infects rice, wheat, barley, and millet. Guided by these metabolic insights, we demonstrated their practical application by using two different small-molecule inhibitors of sphingolipid biosynthesis enzymes to successfully block the pathogenicity of M. oryzae. Our study thus defines the sphingolipid biosynthesis pathway as a key step and potential target that can be exploited for the development of antifungal agents. Furthermore, future investigations that exploit such important metabolic intermediates will further deepen our basic understanding of the molecular mechanisms underlying the establishment of fungal blast disease in important cereal crops.Xiao-Hong LiuShuang LiangYun-Yun WeiXue-Ming ZhuLin LiPing-Ping LiuQing-Xia ZhengHui-Na ZhouYong ZhangLi-Juan MaoCaroline Mota FernandesMaurizio Del PoetaNaweed I. NaqviFu-Cheng LinAmerican Society for Microbiologyarticleappressorium developmentearly sphingolipid signalinginducermetabolomics analysispathogenicityrice blast fungusMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	appressorium development early sphingolipid signaling inducer metabolomics analysis pathogenicity rice blast fungus Microbiology QR1-502
spellingShingle	appressorium development early sphingolipid signaling inducer metabolomics analysis pathogenicity rice blast fungus Microbiology QR1-502 Xiao-Hong Liu Shuang Liang Yun-Yun Wei Xue-Ming Zhu Lin Li Ping-Ping Liu Qing-Xia Zheng Hui-Na Zhou Yong Zhang Li-Juan Mao Caroline Mota Fernandes Maurizio Del Poeta Naweed I. Naqvi Fu-Cheng Lin Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
description	ABSTRACT The blast fungus initiates infection using a heavily melanized, dome-shaped infection structure known as the appressorium, which forcibly ruptures the cuticle to enter the rice leaf tissue. How this process takes place remains not fully understood. Here, we used untargeted metabolomics analyses to profile the metabolome of developing appressoria and identified significant changes in six key metabolic pathways, including early sphingolipid biosynthesis. Analyses employing small molecule inhibitors, gene disruption, or genetic and chemical complementation demonstrated that ceramide compounds of the sphingolipid biosynthesis pathway are essential for normal appressorial development controlled by mitosis. In addition, ceramide was found to act upstream from the protein kinase C-mediated cell wall integrity pathway during appressorium repolarization and pathogenicity in rice blast. Further discovery of the sphingolipid biosynthesis pathway revealed that glucosylceramide (GlcCer) synthesized by ceramide is the key substance affecting the pathogenicity of Magnaporthe oryzae. Our results provide new insights into the chemical moieties involved in the infection-related signaling networks, thereby revealing a potential target for the development of novel control agents against the major disease of rice and other cereals. IMPORTANCE Our untargeted analysis of metabolomics throughout the course of pathogenic development gave us an unprecedented high-resolution view of major shifts in metabolism that occur in the topmost fungal pathogen that infects rice, wheat, barley, and millet. Guided by these metabolic insights, we demonstrated their practical application by using two different small-molecule inhibitors of sphingolipid biosynthesis enzymes to successfully block the pathogenicity of M. oryzae. Our study thus defines the sphingolipid biosynthesis pathway as a key step and potential target that can be exploited for the development of antifungal agents. Furthermore, future investigations that exploit such important metabolic intermediates will further deepen our basic understanding of the molecular mechanisms underlying the establishment of fungal blast disease in important cereal crops.
format	article
author	Xiao-Hong Liu Shuang Liang Yun-Yun Wei Xue-Ming Zhu Lin Li Ping-Ping Liu Qing-Xia Zheng Hui-Na Zhou Yong Zhang Li-Juan Mao Caroline Mota Fernandes Maurizio Del Poeta Naweed I. Naqvi Fu-Cheng Lin
author_facet	Xiao-Hong Liu Shuang Liang Yun-Yun Wei Xue-Ming Zhu Lin Li Ping-Ping Liu Qing-Xia Zheng Hui-Na Zhou Yong Zhang Li-Juan Mao Caroline Mota Fernandes Maurizio Del Poeta Naweed I. Naqvi Fu-Cheng Lin
author_sort	Xiao-Hong Liu
title	Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_short	Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_full	Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_fullStr	Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_full_unstemmed	Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_sort	metabolomics analysis identifies sphingolipids as key signaling moieties in appressorium morphogenesis and function in <named-content content-type="genus-species">magnaporthe oryzae</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/c3495fadcb6345b39a5b88071cf52395
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Metabolomics Analysis Identifies Sphingolipids as Key Signaling Moieties in Appressorium Morphogenesis and Function in <named-content content-type="genus-species">Magnaporthe oryzae</named-content>

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