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

Abstract 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. sol...

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Main Authors: Jia Jiang, Xuhao Guo, Huanhuan Tan, Mingya Ding, Fangming Liu, Zhihui Yang, Jiehua Zhu
Format: Article
Language:English
Published: BMC 2023-03-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04103-3
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author Jia Jiang
Xuhao Guo
Huanhuan Tan
Mingya Ding
Fangming Liu
Zhihui Yang
Jiehua Zhu
author_facet Jia Jiang
Xuhao Guo
Huanhuan Tan
Mingya Ding
Fangming Liu
Zhihui Yang
Jiehua Zhu
author_sort Jia Jiang
collection DOAJ
description Abstract 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.
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spelling doaj.art-9862c2e9675049ef8b811c346491d1c92023-03-22T10:49:52ZengBMCBMC Plant Biology1471-22292023-03-0123111410.1186/s12870-023-04103-3Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potatoJia Jiang0Xuhao Guo1Huanhuan Tan2Mingya Ding3Fangming Liu4Zhihui Yang5Jiehua Zhu6College of Plant Protection, Hebei Agricultural UniversityDepartment of Plant Protection, College of Horticulture and Plant Protection, Henan University of Science and TechnologyDepartment of Plant Protection, College of Horticulture and Plant Protection, Henan University of Science and TechnologyPotato Research Institute of Weichang Manchu and Mongolian Autonomous CountyPotato Research Institute of Weichang Manchu and Mongolian Autonomous CountyCollege of Plant Protection, Hebei Agricultural UniversityCollege of Plant Protection, Hebei Agricultural UniversityAbstract 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.https://doi.org/10.1186/s12870-023-04103-3Alternaria solaniEarly blightRNA-sequencingTranscriptomic analysis
spellingShingle Jia Jiang
Xuhao Guo
Huanhuan Tan
Mingya Ding
Fangming Liu
Zhihui Yang
Jiehua Zhu
Transcriptome sequencing leads to an improved understanding of the infection mechanism of Alternaria solani in potato
BMC Plant Biology
Alternaria solani
Early blight
RNA-sequencing
Transcriptomic analysis
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 Alternaria solani
Early blight
RNA-sequencing
Transcriptomic analysis
url https://doi.org/10.1186/s12870-023-04103-3
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