Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis

Abstract Powdery mildew (PM) fungi are biotrophic pathogens that rely on living hosts to survive and thrive. However, their colonization is restricted by host defenses at both the penetration and post-penetration stages. The tobacco PM strain Golovinomyces cichoracearum (Gc) SICAU1 has overcome pene...

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Main Authors: Ran Li, Ling-Li Zhang, Xue-Mei Yang, Xiao-Long Cao, Ying-Ge Wang, Xian-Feng Ma, Viswanathan Chandran, Jing Fan, Hui Yang, Jing Shang, Ji-Qun Zhao, Shunyuan Xiao, Yan Li, Wen-Ming Wang
Format: Article
Language:English
Published: BMC 2019-02-01
Series:Phytopathology Research
Subjects:
Online Access:http://link.springer.com/article/10.1186/s42483-019-0012-z
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spelling doaj-6b210856e33543d38cc735ba79e08f152020-11-25T01:41:10ZengBMCPhytopathology Research2524-41672019-02-011111610.1186/s42483-019-0012-zTranscriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in ArabidopsisRan Li0Ling-Li Zhang1Xue-Mei Yang2Xiao-Long Cao3Ying-Ge Wang4Xian-Feng Ma5Viswanathan Chandran6Jing Fan7Hui Yang8Jing Shang9Ji-Qun Zhao10Shunyuan Xiao11Yan Li12Wen-Ming Wang13Rice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangInstitute for Bioscience and Biotechnology Research & Department of Plant Science and Landscape Architecture, University of MarylandRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangRice Research Institute and Research Center for Crop Disease and Insect Pests, Sichuan Agricultural University at WenjiangAbstract Powdery mildew (PM) fungi are biotrophic pathogens that rely on living hosts to survive and thrive. However, their colonization is restricted by host defenses at both the penetration and post-penetration stages. The tobacco PM strain Golovinomyces cichoracearum (Gc) SICAU1 has overcome penetration resistance of Arabidopsis but its growth is arrested by post-penetration resistance. While Gc SICAU1 only poorly grows in Arabidopsis Col-0 wild-type plants, it can sustainably grow for more than 20 days on the same infected leaves of the double mutant pad4–1 sid2–1 that is defective in both the synthesis and signaling of salicylic acid (SA). To understand the underlying molecular mechanisms, we conducted a comparative transcriptome analysis between Col-0 and pad4–1 sid2–1 in response to Gc SICAU1. We found that 4811 genes were differentially expressed more than four-fold between any two of the measured seven time points (0, 1, 3, 6, 8, 10 and 12 days post-inoculation). Gene expression pattern analysis suggests that differential expression of 348 genes and 190 genes may explain resistance in Col-0 and susceptibility in pad4–1 sid2–1, respectively. Gene Ontology (GO) analysis suggests that Gc SICAU1 might be arrested in Col-0 by both pattern-triggered immunity and SA-dependent defense. By contrast, its sustained growth in pad4–1 sid2–1 may be attributable to the activation of a detoxification pathway that is normally repressed by the SA-signaling pathway. Taken together, our results suggest that multiple distinct, yet interconnected pathways control the growth of tobacco powdery mildew in Arabidopsis.http://link.springer.com/article/10.1186/s42483-019-0012-zBasal defenseSA-signalingPost-penetration defensePattern-triggered immunityGolovinomyces cichoracearum SICAU1Detoxification
collection DOAJ
language English
format Article
sources DOAJ
author Ran Li
Ling-Li Zhang
Xue-Mei Yang
Xiao-Long Cao
Ying-Ge Wang
Xian-Feng Ma
Viswanathan Chandran
Jing Fan
Hui Yang
Jing Shang
Ji-Qun Zhao
Shunyuan Xiao
Yan Li
Wen-Ming Wang
spellingShingle Ran Li
Ling-Li Zhang
Xue-Mei Yang
Xiao-Long Cao
Ying-Ge Wang
Xian-Feng Ma
Viswanathan Chandran
Jing Fan
Hui Yang
Jing Shang
Ji-Qun Zhao
Shunyuan Xiao
Yan Li
Wen-Ming Wang
Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
Phytopathology Research
Basal defense
SA-signaling
Post-penetration defense
Pattern-triggered immunity
Golovinomyces cichoracearum SICAU1
Detoxification
author_facet Ran Li
Ling-Li Zhang
Xue-Mei Yang
Xiao-Long Cao
Ying-Ge Wang
Xian-Feng Ma
Viswanathan Chandran
Jing Fan
Hui Yang
Jing Shang
Ji-Qun Zhao
Shunyuan Xiao
Yan Li
Wen-Ming Wang
author_sort Ran Li
title Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
title_short Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
title_full Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
title_fullStr Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
title_full_unstemmed Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis
title_sort transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in arabidopsis
publisher BMC
series Phytopathology Research
issn 2524-4167
publishDate 2019-02-01
description Abstract Powdery mildew (PM) fungi are biotrophic pathogens that rely on living hosts to survive and thrive. However, their colonization is restricted by host defenses at both the penetration and post-penetration stages. The tobacco PM strain Golovinomyces cichoracearum (Gc) SICAU1 has overcome penetration resistance of Arabidopsis but its growth is arrested by post-penetration resistance. While Gc SICAU1 only poorly grows in Arabidopsis Col-0 wild-type plants, it can sustainably grow for more than 20 days on the same infected leaves of the double mutant pad4–1 sid2–1 that is defective in both the synthesis and signaling of salicylic acid (SA). To understand the underlying molecular mechanisms, we conducted a comparative transcriptome analysis between Col-0 and pad4–1 sid2–1 in response to Gc SICAU1. We found that 4811 genes were differentially expressed more than four-fold between any two of the measured seven time points (0, 1, 3, 6, 8, 10 and 12 days post-inoculation). Gene expression pattern analysis suggests that differential expression of 348 genes and 190 genes may explain resistance in Col-0 and susceptibility in pad4–1 sid2–1, respectively. Gene Ontology (GO) analysis suggests that Gc SICAU1 might be arrested in Col-0 by both pattern-triggered immunity and SA-dependent defense. By contrast, its sustained growth in pad4–1 sid2–1 may be attributable to the activation of a detoxification pathway that is normally repressed by the SA-signaling pathway. Taken together, our results suggest that multiple distinct, yet interconnected pathways control the growth of tobacco powdery mildew in Arabidopsis.
topic Basal defense
SA-signaling
Post-penetration defense
Pattern-triggered immunity
Golovinomyces cichoracearum SICAU1
Detoxification
url http://link.springer.com/article/10.1186/s42483-019-0012-z
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