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Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease
BACKGROUND: Nerium indicum Mill. is an ornamental plant that is found in parks, riversides, lakesides, and scenic areas in China and other parts of the world. Our recent survey indicated the prevalence of witches’ broom disease (WBD) in Guangdong, China. To find out the possible defense strategies a...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9199210/ https://www.ncbi.nlm.nih.gov/pubmed/35701735 http://dx.doi.org/10.1186/s12870-022-03672-z |
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author | Wang, Shengjie Wang, Shengkun Li, Ming Su, Yuhang Sun, Zhan Ma, Haibin |
author_facet | Wang, Shengjie Wang, Shengkun Li, Ming Su, Yuhang Sun, Zhan Ma, Haibin |
author_sort | Wang, Shengjie |
collection | PubMed |
description | BACKGROUND: Nerium indicum Mill. is an ornamental plant that is found in parks, riversides, lakesides, and scenic areas in China and other parts of the world. Our recent survey indicated the prevalence of witches’ broom disease (WBD) in Guangdong, China. To find out the possible defense strategies against WBD, we performed a MiSeq based ITS sequencing to identify the possible casual organism, then did a de novo transcriptome sequencing and metabolome profiling in the phloem and stem tip of N. indicum plants suffering from WBD compared to healthy ones. RESULTS: The survey showed that Wengyuen county and Zengcheng district had the highest disease incidence rates. The most prevalent microbial species in the diseased tissues was Cophinforma mamane. The transcriptome sequencing resulted in the identification of 191,224 unigenes of which 142,396 could be annotated. There were 19,031 and 13,284 differentially expressed genes (DEGs) between diseased phloem (NOWP) and healthy phloem (NOHP), and diseased stem (NOWS) and healthy stem (NOHS), respectively. The DEGs were enriched in MAPK-signaling (plant), plant-pathogen interaction, plant-hormone signal transduction, phenylpropanoid and flavonoid biosynthesis, linoleic acid and α-linoleic acid metabolism pathways. Particularly, we found that N. indicum plants activated the phytohormone signaling, MAPK-signaling cascade, defense related proteins, and the biosynthesis of phenylpropanoids and flavonoids as defense responses to the pathogenic infection. The metabolome profiling identified 586 metabolites of which 386 and 324 metabolites were differentially accumulated in NOHP vs NOWP and NOHS and NOWS, respectively. The differential accumulation of metabolites related to phytohormone signaling, linoleic acid metabolism, phenylpropanoid and flavonoid biosynthesis, nicotinate and nicotinamide metabolism, and citrate cycle was observed, indicating the role of these pathways in defense responses against the pathogenic infection. CONCLUSION: Our results showed that Guangdong province has a high incidence of WBD in most of the surveyed areas. C. mamane is suspected to be the causing pathogen of WBD in N. indicum. N. indicum initiated the MAPK-signaling cascade and phytohormone signaling, leading to the activation of pathogen-associated molecular patterns and hypersensitive response. Furthermore, N. indicum accumulated high concentrations of phenolic acids, coumarins and lignans, and flavonoids under WBD. These results provide scientific tools for the formulation of control strategies of WBD in N. indicum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03672-z. |
format | Online Article Text |
id | pubmed-9199210 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91992102022-06-16 Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease Wang, Shengjie Wang, Shengkun Li, Ming Su, Yuhang Sun, Zhan Ma, Haibin BMC Plant Biol Research BACKGROUND: Nerium indicum Mill. is an ornamental plant that is found in parks, riversides, lakesides, and scenic areas in China and other parts of the world. Our recent survey indicated the prevalence of witches’ broom disease (WBD) in Guangdong, China. To find out the possible defense strategies against WBD, we performed a MiSeq based ITS sequencing to identify the possible casual organism, then did a de novo transcriptome sequencing and metabolome profiling in the phloem and stem tip of N. indicum plants suffering from WBD compared to healthy ones. RESULTS: The survey showed that Wengyuen county and Zengcheng district had the highest disease incidence rates. The most prevalent microbial species in the diseased tissues was Cophinforma mamane. The transcriptome sequencing resulted in the identification of 191,224 unigenes of which 142,396 could be annotated. There were 19,031 and 13,284 differentially expressed genes (DEGs) between diseased phloem (NOWP) and healthy phloem (NOHP), and diseased stem (NOWS) and healthy stem (NOHS), respectively. The DEGs were enriched in MAPK-signaling (plant), plant-pathogen interaction, plant-hormone signal transduction, phenylpropanoid and flavonoid biosynthesis, linoleic acid and α-linoleic acid metabolism pathways. Particularly, we found that N. indicum plants activated the phytohormone signaling, MAPK-signaling cascade, defense related proteins, and the biosynthesis of phenylpropanoids and flavonoids as defense responses to the pathogenic infection. The metabolome profiling identified 586 metabolites of which 386 and 324 metabolites were differentially accumulated in NOHP vs NOWP and NOHS and NOWS, respectively. The differential accumulation of metabolites related to phytohormone signaling, linoleic acid metabolism, phenylpropanoid and flavonoid biosynthesis, nicotinate and nicotinamide metabolism, and citrate cycle was observed, indicating the role of these pathways in defense responses against the pathogenic infection. CONCLUSION: Our results showed that Guangdong province has a high incidence of WBD in most of the surveyed areas. C. mamane is suspected to be the causing pathogen of WBD in N. indicum. N. indicum initiated the MAPK-signaling cascade and phytohormone signaling, leading to the activation of pathogen-associated molecular patterns and hypersensitive response. Furthermore, N. indicum accumulated high concentrations of phenolic acids, coumarins and lignans, and flavonoids under WBD. These results provide scientific tools for the formulation of control strategies of WBD in N. indicum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03672-z. BioMed Central 2022-06-14 /pmc/articles/PMC9199210/ /pubmed/35701735 http://dx.doi.org/10.1186/s12870-022-03672-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Wang, Shengjie Wang, Shengkun Li, Ming Su, Yuhang Sun, Zhan Ma, Haibin Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title | Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title_full | Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title_fullStr | Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title_full_unstemmed | Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title_short | Combined transcriptome and metabolome analysis of Nerium indicum L. elaborates the key pathways that are activated in response to witches’ broom disease |
title_sort | combined transcriptome and metabolome analysis of nerium indicum l. elaborates the key pathways that are activated in response to witches’ broom disease |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9199210/ https://www.ncbi.nlm.nih.gov/pubmed/35701735 http://dx.doi.org/10.1186/s12870-022-03672-z |
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