Agrobacteria reprogram virulence gene expression by controlled release of host-conjugated signals

It is highly intriguing how bacterial pathogens can quickly shut down energy-costly infection machinery once successful infection is established. This study depicts that mutation of repressor SghR increases the expression of hydrolase SghA in Agrobacterium tumefaciens, which releases plant defense s...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 116; no. 44; pp. 22331 - 22340
Main Authors Wang, Chao, Ye, Fuzhou, Chang, Changqing, Liu, Xiaoling, Wang, Jianhe, Wang, Jinpei, Yan, Xin-Fu, Fu, Qinqin, Zhou, Jianuan, Chen, Shaohua, Gao, Yong-Gui, Zhang, Lian-Hui
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 29.10.2019
SeriesPNAS Plus
Subjects
Agrobacterium tumefaciens - genetics
Agrobacterium tumefaciens - pathogenicity
Arabidopsis - metabolism
Arabidopsis - microbiology
Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biological Sciences
Controlled release
Disruption
Gene expression
Host-Pathogen Interactions
Hydrolase
Hydrolases - genetics
Hydrolases - metabolism
Infections
Metabolites
Mutation
PNAS Plus
Salicylic acid
Salicylic Acid - metabolism
Shutdowns
Signal Transduction
Sucrose
Sucrose - metabolism
Sugar
Transcription Factors - genetics
Transcription Factors - metabolism
Tumors
Virulence
Virulence Factors - genetics
Agrobacterium
glucosidase
cost–pathogen interaction
sucrose
chemical signaling
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Summary:It is highly intriguing how bacterial pathogens can quickly shut down energy-costly infection machinery once successful infection is established. This study depicts that mutation of repressor SghR increases the expression of hydrolase SghA in Agrobacterium tumefaciens, which releases plant defense signal salicylic acid (SA) from its storage form SA β-glucoside (SAG). Addition of SA substantially reduces gene expression of bacterial virulence. Bacterial vir genes and sghA are differentially transcribed at early and later infection stages, respectively. Plant metabolite sucrose is a signal ligand that inactivates SghR and consequently induces sghA expression. Disruption of sghA leads to increased vir expression in planta and enhances tumor formation whereas mutation of sghR decreases vir expression and tumor formation. These results depict a remarkable mechanism by which A. tumefaciens taps on the reserved pool of plant signal SA to reprogram its virulence upon establishment of infection.
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Author contributions: C.W., Y.-G.G., and L.-H.Z. designed research; C.W., F.Y., C.C., X.L., Jianhe Wang, Jinpei Wang, X.-F.Y., Q.F., J.Z., and S.C. performed research; L.-H.Z. contributed new reagents/analytic tools; C.W., F.Y., Y.-G.G., and L.-H.Z. analyzed data; and C.W., Y.-G.G., and L.-H.Z. wrote the paper.
Edited by P. Zambryski, University of California, Berkeley, CA, and approved September 18, 2019 (received for review March 4, 2019)
1C.W., F.Y., and C.C. contributed equally to this work.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.1903695116