Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection

<i>Mikania micrantha</i> is one of the worst invasive species globally and can cause significant negative impacts on agricultural and forestry economics, particularly in Asia and the Pacific region. The rust <i>Puccinia spegazzinii</i> has been used successfully as a biologic...

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Main Authors: Xinghai Ren, Guangzhong Zhang, Mengjiao Jin, Fanghao Wan, Michael D. Day, Wanqiang Qian, Bo Liu
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/3/678
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author Xinghai Ren
Guangzhong Zhang
Mengjiao Jin
Fanghao Wan
Michael D. Day
Wanqiang Qian
Bo Liu
author_facet Xinghai Ren
Guangzhong Zhang
Mengjiao Jin
Fanghao Wan
Michael D. Day
Wanqiang Qian
Bo Liu
author_sort Xinghai Ren
collection DOAJ
description <i>Mikania micrantha</i> is one of the worst invasive species globally and can cause significant negative impacts on agricultural and forestry economics, particularly in Asia and the Pacific region. The rust <i>Puccinia spegazzinii</i> has been used successfully as a biological control agent in several countries to help manage <i>M. micrantha</i>. However, the response mechanisms of <i>M. micrantha</i> to <i>P. spegazzinii</i> infection have never been studied. To investigate the response of <i>M. micrantha</i> to infection by <i>P. spegazzinii</i>, an integrated analysis of metabolomics and transcriptomics was performed. The levels of 74 metabolites, including organic acids, amino acids, and secondary metabolites in <i>M. micrantha</i> infected with <i>P. spegazzinii</i>, were significantly different compared to those in plants that were not infected. After <i>P. spegazzinii</i> infection, the expression of the TCA cycle gene was significantly induced to participate in energy biosynthesis and produce more ATP. The content of most amino acids, such as L-isoleucine, L-tryptophan and L-citrulline, increased. In addition, phytoalexins, such as maackiain, nobiletin, vasicin, arachidonic acid, and JA-Ile, accumulated in <i>M. micrantha</i>. A total of 4978 differentially expressed genes were identified in <i>M. micrantha</i> infected by <i>P. spegazzinii</i>. Many key genes of <i>M. micrantha</i> in the PTI (pattern-triggered immunity) and ETI (effector-triggered immunity) pathways showed significantly higher expression under <i>P. spegazzinii</i> infection. Through these reactions, <i>M. micrantha</i> is able to resist the infection of <i>P. spegazzinii</i> and maintain its growth. These results are helpful for us to understand the changes in metabolites and gene expression in <i>M. micrantha</i> after being infected by <i>P. spegazzinii</i>. Our results can provide a theoretical basis for weakening the defense response of <i>M. micrantha</i> to <i>P. spegazzinii</i>, and for <i>P. spegazzinii</i> as a long-term biological control agent of <i>M. micrantha</i>.
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spelling doaj.art-3568d523bb644ca9803390d8deabeaac2023-12-01T01:22:31ZengMDPI AGMicroorganisms2076-26072023-03-0111367810.3390/microorganisms11030678Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> InfectionXinghai Ren0Guangzhong Zhang1Mengjiao Jin2Fanghao Wan3Michael D. Day4Wanqiang Qian5Bo Liu6Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, ChinaDepartment of Agriculture and Fisheries, Ecosciences Precinct, GPO Box 267, Brisbane, QLD 4001, AustraliaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, China<i>Mikania micrantha</i> is one of the worst invasive species globally and can cause significant negative impacts on agricultural and forestry economics, particularly in Asia and the Pacific region. The rust <i>Puccinia spegazzinii</i> has been used successfully as a biological control agent in several countries to help manage <i>M. micrantha</i>. However, the response mechanisms of <i>M. micrantha</i> to <i>P. spegazzinii</i> infection have never been studied. To investigate the response of <i>M. micrantha</i> to infection by <i>P. spegazzinii</i>, an integrated analysis of metabolomics and transcriptomics was performed. The levels of 74 metabolites, including organic acids, amino acids, and secondary metabolites in <i>M. micrantha</i> infected with <i>P. spegazzinii</i>, were significantly different compared to those in plants that were not infected. After <i>P. spegazzinii</i> infection, the expression of the TCA cycle gene was significantly induced to participate in energy biosynthesis and produce more ATP. The content of most amino acids, such as L-isoleucine, L-tryptophan and L-citrulline, increased. In addition, phytoalexins, such as maackiain, nobiletin, vasicin, arachidonic acid, and JA-Ile, accumulated in <i>M. micrantha</i>. A total of 4978 differentially expressed genes were identified in <i>M. micrantha</i> infected by <i>P. spegazzinii</i>. Many key genes of <i>M. micrantha</i> in the PTI (pattern-triggered immunity) and ETI (effector-triggered immunity) pathways showed significantly higher expression under <i>P. spegazzinii</i> infection. Through these reactions, <i>M. micrantha</i> is able to resist the infection of <i>P. spegazzinii</i> and maintain its growth. These results are helpful for us to understand the changes in metabolites and gene expression in <i>M. micrantha</i> after being infected by <i>P. spegazzinii</i>. Our results can provide a theoretical basis for weakening the defense response of <i>M. micrantha</i> to <i>P. spegazzinii</i>, and for <i>P. spegazzinii</i> as a long-term biological control agent of <i>M. micrantha</i>.https://www.mdpi.com/2076-2607/11/3/678transcriptomemetabolomeimmune responsebiological controlPucciniales
spellingShingle Xinghai Ren
Guangzhong Zhang
Mengjiao Jin
Fanghao Wan
Michael D. Day
Wanqiang Qian
Bo Liu
Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
Microorganisms
transcriptome
metabolome
immune response
biological control
Pucciniales
title Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
title_full Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
title_fullStr Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
title_full_unstemmed Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
title_short Metabolomics and Transcriptomics Reveal the Response Mechanisms of <i>Mikania micrantha</i> to <i>Puccinia spegazzinii</i> Infection
title_sort metabolomics and transcriptomics reveal the response mechanisms of i mikania micrantha i to i puccinia spegazzinii i infection
topic transcriptome
metabolome
immune response
biological control
Pucciniales
url https://www.mdpi.com/2076-2607/11/3/678
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