Cargando…

The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis

Many species of plant-pathogenic gram-negative bacteria deploy the type III (T3) secretion system to secrete virulence components, which are mostly characteristic of protein effectors targeting the cytosol of the plant cell following secretion. Xanthomonas oryzae pv. oryzae (Xoo), a rice pathogen ca...

Descripción completa

Detalles Bibliográficos
Autores principales: Sheikh, Taha Majid Mahmood, Zhang, Liyuan, Zubair, Muhammad, Hanif, Alvina, Li, Ping, Farzand, Ayaz, Ali, Haider, Bilal, Muhammad Saqib, Hu, Yiqun, Chen, Xiaochen, Song, Congfeng, Dong, Hansong, Zhang, Meixiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6921029/
https://www.ncbi.nlm.nih.gov/pubmed/31752133
http://dx.doi.org/10.3390/microorganisms7110572
_version_ 1783481069686751232
author Sheikh, Taha Majid Mahmood
Zhang, Liyuan
Zubair, Muhammad
Hanif, Alvina
Li, Ping
Farzand, Ayaz
Ali, Haider
Bilal, Muhammad Saqib
Hu, Yiqun
Chen, Xiaochen
Song, Congfeng
Dong, Hansong
Zhang, Meixiang
author_facet Sheikh, Taha Majid Mahmood
Zhang, Liyuan
Zubair, Muhammad
Hanif, Alvina
Li, Ping
Farzand, Ayaz
Ali, Haider
Bilal, Muhammad Saqib
Hu, Yiqun
Chen, Xiaochen
Song, Congfeng
Dong, Hansong
Zhang, Meixiang
author_sort Sheikh, Taha Majid Mahmood
collection PubMed
description Many species of plant-pathogenic gram-negative bacteria deploy the type III (T3) secretion system to secrete virulence components, which are mostly characteristic of protein effectors targeting the cytosol of the plant cell following secretion. Xanthomonas oryzae pv. oryzae (Xoo), a rice pathogen causing bacterial blight disease, uses the T3 accessory protein HrpE to assemble the pilus pathway, which in turn secretes transcription activator-like (TAL) effectors. The hrpE gene can execute extensive physiological and pathological functions beyond effector secretion. As evidenced in this study, when the hrpE gene was deleted from the Xoo genome, the bacteria incur seriouimpairments in multiplication, motility, and virulence. The virulence nullification is attributed to reduced secretion and translocation of PthXo1, which is a TAL effector that determines the bacterial virulence in the susceptible rice varieties. When the HrpE protein produced by prokaryotic expression is applied to plants, the recombinant protein is highly effective at inducing the defense response. Moreover, leaf photosynthesis efficiency is enhanced in HrpE-treated plants. These results provide experimental avenues to modulate the plant defense and growth tradeoff by manipulating a bacterial T3 accessory protein.
format Online
Article
Text
id pubmed-6921029
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-69210292019-12-24 The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis Sheikh, Taha Majid Mahmood Zhang, Liyuan Zubair, Muhammad Hanif, Alvina Li, Ping Farzand, Ayaz Ali, Haider Bilal, Muhammad Saqib Hu, Yiqun Chen, Xiaochen Song, Congfeng Dong, Hansong Zhang, Meixiang Microorganisms Article Many species of plant-pathogenic gram-negative bacteria deploy the type III (T3) secretion system to secrete virulence components, which are mostly characteristic of protein effectors targeting the cytosol of the plant cell following secretion. Xanthomonas oryzae pv. oryzae (Xoo), a rice pathogen causing bacterial blight disease, uses the T3 accessory protein HrpE to assemble the pilus pathway, which in turn secretes transcription activator-like (TAL) effectors. The hrpE gene can execute extensive physiological and pathological functions beyond effector secretion. As evidenced in this study, when the hrpE gene was deleted from the Xoo genome, the bacteria incur seriouimpairments in multiplication, motility, and virulence. The virulence nullification is attributed to reduced secretion and translocation of PthXo1, which is a TAL effector that determines the bacterial virulence in the susceptible rice varieties. When the HrpE protein produced by prokaryotic expression is applied to plants, the recombinant protein is highly effective at inducing the defense response. Moreover, leaf photosynthesis efficiency is enhanced in HrpE-treated plants. These results provide experimental avenues to modulate the plant defense and growth tradeoff by manipulating a bacterial T3 accessory protein. MDPI 2019-11-18 /pmc/articles/PMC6921029/ /pubmed/31752133 http://dx.doi.org/10.3390/microorganisms7110572 Text en © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Sheikh, Taha Majid Mahmood
Zhang, Liyuan
Zubair, Muhammad
Hanif, Alvina
Li, Ping
Farzand, Ayaz
Ali, Haider
Bilal, Muhammad Saqib
Hu, Yiqun
Chen, Xiaochen
Song, Congfeng
Dong, Hansong
Zhang, Meixiang
The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title_full The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title_fullStr The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title_full_unstemmed The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title_short The Type III Accessory Protein HrpE of Xanthomonas oryzae pv. oryzae Surpasses the Secretion Role, and Enhances Plant Resistance and Photosynthesis
title_sort type iii accessory protein hrpe of xanthomonas oryzae pv. oryzae surpasses the secretion role, and enhances plant resistance and photosynthesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6921029/
https://www.ncbi.nlm.nih.gov/pubmed/31752133
http://dx.doi.org/10.3390/microorganisms7110572
work_keys_str_mv AT sheikhtahamajidmahmood thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zhangliyuan thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zubairmuhammad thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT hanifalvina thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT liping thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT farzandayaz thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT alihaider thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT bilalmuhammadsaqib thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT huyiqun thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT chenxiaochen thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT songcongfeng thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT donghansong thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zhangmeixiang thetypeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT sheikhtahamajidmahmood typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zhangliyuan typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zubairmuhammad typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT hanifalvina typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT liping typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT farzandayaz typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT alihaider typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT bilalmuhammadsaqib typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT huyiqun typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT chenxiaochen typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT songcongfeng typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT donghansong typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis
AT zhangmeixiang typeiiiaccessoryproteinhrpeofxanthomonasoryzaepvoryzaesurpassesthesecretionroleandenhancesplantresistanceandphotosynthesis