Cargando…

Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato

BACKGROUND: Alternaria solani (A. solani), the main pathogen of potato early blight, causes serious yield reductions every year. The application of fungicides is the most common and effective method of controlling Alternaria-caused diseases. The differentially expressed transcripts of A. solani infe...

Descripción completa

Detalles Bibliográficos
Autores principales: Jiang, Jia, Guo, Xuhao, Tan, Huanhuan, Ding, Mingya, Liu, Fangming, Yang, Zhihui, Zhu, Jiehua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976505/
https://www.ncbi.nlm.nih.gov/pubmed/36859112
http://dx.doi.org/10.1186/s12870-023-04103-3
_version_ 1784899098486243328
author Jiang, Jia
Guo, Xuhao
Tan, Huanhuan
Ding, Mingya
Liu, Fangming
Yang, Zhihui
Zhu, Jiehua
author_facet Jiang, Jia
Guo, Xuhao
Tan, Huanhuan
Ding, Mingya
Liu, Fangming
Yang, Zhihui
Zhu, Jiehua
author_sort Jiang, Jia
collection PubMed
description BACKGROUND: Alternaria solani (A. solani), the main pathogen of potato early blight, causes serious yield reductions every year. The application of fungicides is the most common and effective method of controlling Alternaria-caused diseases. The differentially expressed transcripts of A. solani infecting potato were identified, revealing a group of valuable candidate genes for a systematic analysis to increase the understanding of the molecular pathogenesis of A. solani, and providing scientific data for formulating additional measures to prevent and control potato early blight. In this study, a deep RNA-sequencing approach was applied to gain insights into A. solani pathogenesis. At 3, 4, and 5 days post inoculation (dpi), RNA samples from the susceptible potato cultivar Favorita infected with A. solani strain HWC-168, were sequenced and utilized for transcriptome analysis, and compared to the transcriptome obtained 0 dpi. RESULTS: A total of 4430 (2167 upregulated, 2263 downregulated), 4736 (2312 upregulated, 2424 downregulated), and 5043 (2411 upregulated, 2632 downregulated) genes were differentially expressed 3, 4 and 5 dpi, respectively, compared with genes analysed at 0 dpi. KEGG enrichment analysis showed that genes involved in the pathways of amino acid metabolism, glucose metabolism, and enzyme activity were significantly differentially expressed at the late infection stage. Correspondingly, symptoms developed rapidly during the late stage of A. solani infection. In addition, a short time-series expression miner (STEM) assay was performed to analyse the gene expression patterns of A. solani and Profile 17 and 19 showed significant change trends 3, 4 and 5 dpi. Both profiles, but especially Profile 17, included enzymes, including transferases, oxidoreductases, hydrolases and carbohydrate-active enzymes (CAZYmes), which may play important roles in late fungal infection. Furthermore, possible candidate effectors were identified through the adopted pipelines, with 137 differentially expressed small secreted proteins identified, including some enzymes and proteins with unknown functions. CONCLUSIONS: Collectively, the data presented in this study show that amino acid metabolism, and glucose metabolism pathways, and specific pathway-related enzymes may be key putative pathogenic factors, and play important roles in late stage A. solani infection. These results contribute to a broader base of knowledge of A. solani pathogenesis in potato, as indicated by the transcriptional level analysis, and provide clues for determining the effectors of A. solani infection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04103-3.
format Online
Article
Text
id pubmed-9976505
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-99765052023-03-02 Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato Jiang, Jia Guo, Xuhao Tan, Huanhuan Ding, Mingya Liu, Fangming Yang, Zhihui Zhu, Jiehua BMC Plant Biol Research BACKGROUND: Alternaria solani (A. solani), the main pathogen of potato early blight, causes serious yield reductions every year. The application of fungicides is the most common and effective method of controlling Alternaria-caused diseases. The differentially expressed transcripts of A. solani infecting potato were identified, revealing a group of valuable candidate genes for a systematic analysis to increase the understanding of the molecular pathogenesis of A. solani, and providing scientific data for formulating additional measures to prevent and control potato early blight. In this study, a deep RNA-sequencing approach was applied to gain insights into A. solani pathogenesis. At 3, 4, and 5 days post inoculation (dpi), RNA samples from the susceptible potato cultivar Favorita infected with A. solani strain HWC-168, were sequenced and utilized for transcriptome analysis, and compared to the transcriptome obtained 0 dpi. RESULTS: A total of 4430 (2167 upregulated, 2263 downregulated), 4736 (2312 upregulated, 2424 downregulated), and 5043 (2411 upregulated, 2632 downregulated) genes were differentially expressed 3, 4 and 5 dpi, respectively, compared with genes analysed at 0 dpi. KEGG enrichment analysis showed that genes involved in the pathways of amino acid metabolism, glucose metabolism, and enzyme activity were significantly differentially expressed at the late infection stage. Correspondingly, symptoms developed rapidly during the late stage of A. solani infection. In addition, a short time-series expression miner (STEM) assay was performed to analyse the gene expression patterns of A. solani and Profile 17 and 19 showed significant change trends 3, 4 and 5 dpi. Both profiles, but especially Profile 17, included enzymes, including transferases, oxidoreductases, hydrolases and carbohydrate-active enzymes (CAZYmes), which may play important roles in late fungal infection. Furthermore, possible candidate effectors were identified through the adopted pipelines, with 137 differentially expressed small secreted proteins identified, including some enzymes and proteins with unknown functions. CONCLUSIONS: Collectively, the data presented in this study show that amino acid metabolism, and glucose metabolism pathways, and specific pathway-related enzymes may be key putative pathogenic factors, and play important roles in late stage A. solani infection. These results contribute to a broader base of knowledge of A. solani pathogenesis in potato, as indicated by the transcriptional level analysis, and provide clues for determining the effectors of A. solani infection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04103-3. BioMed Central 2023-03-01 /pmc/articles/PMC9976505/ /pubmed/36859112 http://dx.doi.org/10.1186/s12870-023-04103-3 Text en © The Author(s) 2023 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
Jiang, Jia
Guo, Xuhao
Tan, Huanhuan
Ding, Mingya
Liu, Fangming
Yang, Zhihui
Zhu, Jiehua
Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title_full Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title_fullStr Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title_full_unstemmed Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title_short Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
title_sort transcriptome sequencing leads to an improved understanding of the infection mechanism of alternaria solani in potato
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9976505/
https://www.ncbi.nlm.nih.gov/pubmed/36859112
http://dx.doi.org/10.1186/s12870-023-04103-3
work_keys_str_mv AT jiangjia transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT guoxuhao transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT tanhuanhuan transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT dingmingya transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT liufangming transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT yangzhihui transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato
AT zhujiehua transcriptomesequencingleadstoanimprovedunderstandingoftheinfectionmechanismofalternariasolaniinpotato