Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid

Abstract Background We previously identified a plant-derived phenolic compound ortho-coumaric acid (OCA) as an inhibitor of type III secretion system (T3SS) of Xanthomonas oryzae pv. oryzae (Xoo), the pathogen causing bacterial leaf blight of rice, one of the most devastating bacterial diseases of t...

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Main Authors: Susu Fan, Fang Tian, Liwei Fang, Ching-Hong Yang, Chenyang He
Format: Article
Language:English
Published: BMC 2019-07-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-019-1532-5
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author Susu Fan
Fang Tian
Liwei Fang
Ching-Hong Yang
Chenyang He
author_facet Susu Fan
Fang Tian
Liwei Fang
Ching-Hong Yang
Chenyang He
author_sort Susu Fan
collection DOAJ
description Abstract Background We previously identified a plant-derived phenolic compound ortho-coumaric acid (OCA) as an inhibitor of type III secretion system (T3SS) of Xanthomonas oryzae pv. oryzae (Xoo), the pathogen causing bacterial leaf blight of rice, one of the most devastating bacterial diseases of this staple crop worldwide. However, the molecular mechanisms by which OCA suppresses T3SS and the transcriptional responses to the OCA treatments in Xoo remains unclear. Results The present study conducted the RNA-seq-based transcriptomic analysis to reveal changes in gene expression in Xoo in response to 30 min, 1 h, 3 h, and 6 h of OCA treatment. Results showed that OCA significantly inhibited the expression of T3SS genes after 30 min, and the inhibition also existed after 1 h, 3 h, and 6 h. After treatment for 30 min, membrane proteins in the functional category of cellular process was the predominant group affected, indicating that Xoo was in the early stress stage. Over time, more differentially-expressed genes (DEGs) gathered in the functional category of biological process. Analysis of common DEGs at all four of time points revealed the core elements of Xoo during the response to OCA treatment. Notable, a multidrug transporter cluster that consisted of a MarR-family protein (PXO_RS13760), a multidrug RND transporter (PXO_RS13755), a multidrug transporter (PXO_RS13750), and an MFS transporter (PXO_RS13745) were significantly up-regulated at all four of the time points. Although these three transporter genes were not upregulated by OCA in the PXO_RS13760 deletion mutant, the deficiency of PXO_RS13760 in Xoo did not affect T3SS transcript, and OCA still had the ability to inhibit the expression of T3SS in the mutant, suggesting that the MarR-family protein was involved in bacterial responses to OCA, but not direct OCA inhibition of T3SS in Xoo. Conclusions We analyzed the transcriptome of Xoo during OCA treatment at both early and late stages, which revealed the landscape of Xoo responses to OCA at the whole-genome transcription level. A multidrug transporter cluster was identified to be involved in the response process, but had no direct relation to T3SS in Xoo.
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spelling doaj.art-e362d878e1b048199a8993e4d4939ba32022-12-21T18:41:14ZengBMCBMC Microbiology1471-21802019-07-0119111210.1186/s12866-019-1532-5Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acidSusu Fan0Fang Tian1Liwei Fang2Ching-Hong Yang3Chenyang He4State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection, Chinese Academy of Agricultural SciencesDepartment of Biological Sciences, University of Wisconsin-MilwaukeeDepartment of Biological Sciences, University of Wisconsin-MilwaukeeState Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection, Chinese Academy of Agricultural SciencesAbstract Background We previously identified a plant-derived phenolic compound ortho-coumaric acid (OCA) as an inhibitor of type III secretion system (T3SS) of Xanthomonas oryzae pv. oryzae (Xoo), the pathogen causing bacterial leaf blight of rice, one of the most devastating bacterial diseases of this staple crop worldwide. However, the molecular mechanisms by which OCA suppresses T3SS and the transcriptional responses to the OCA treatments in Xoo remains unclear. Results The present study conducted the RNA-seq-based transcriptomic analysis to reveal changes in gene expression in Xoo in response to 30 min, 1 h, 3 h, and 6 h of OCA treatment. Results showed that OCA significantly inhibited the expression of T3SS genes after 30 min, and the inhibition also existed after 1 h, 3 h, and 6 h. After treatment for 30 min, membrane proteins in the functional category of cellular process was the predominant group affected, indicating that Xoo was in the early stress stage. Over time, more differentially-expressed genes (DEGs) gathered in the functional category of biological process. Analysis of common DEGs at all four of time points revealed the core elements of Xoo during the response to OCA treatment. Notable, a multidrug transporter cluster that consisted of a MarR-family protein (PXO_RS13760), a multidrug RND transporter (PXO_RS13755), a multidrug transporter (PXO_RS13750), and an MFS transporter (PXO_RS13745) were significantly up-regulated at all four of the time points. Although these three transporter genes were not upregulated by OCA in the PXO_RS13760 deletion mutant, the deficiency of PXO_RS13760 in Xoo did not affect T3SS transcript, and OCA still had the ability to inhibit the expression of T3SS in the mutant, suggesting that the MarR-family protein was involved in bacterial responses to OCA, but not direct OCA inhibition of T3SS in Xoo. Conclusions We analyzed the transcriptome of Xoo during OCA treatment at both early and late stages, which revealed the landscape of Xoo responses to OCA at the whole-genome transcription level. A multidrug transporter cluster was identified to be involved in the response process, but had no direct relation to T3SS in Xoo.http://link.springer.com/article/10.1186/s12866-019-1532-5Xanthomonas oryzae pv. oryzaeType III secretion systemInhibitorortho-coumaric acidTranscriptome
spellingShingle Susu Fan
Fang Tian
Liwei Fang
Ching-Hong Yang
Chenyang He
Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
BMC Microbiology
Xanthomonas oryzae pv. oryzae
Type III secretion system
Inhibitor
ortho-coumaric acid
Transcriptome
title Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
title_full Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
title_fullStr Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
title_full_unstemmed Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
title_short Transcriptional responses of Xanthomonas oryzae pv. oryzae to type III secretion system inhibitor ortho-coumaric acid
title_sort transcriptional responses of xanthomonas oryzae pv oryzae to type iii secretion system inhibitor ortho coumaric acid
topic Xanthomonas oryzae pv. oryzae
Type III secretion system
Inhibitor
ortho-coumaric acid
Transcriptome
url http://link.springer.com/article/10.1186/s12866-019-1532-5
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