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 in | Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 44; pp. 22331 - 22340 |
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| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
29.10.2019
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| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | 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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| AbstractList | Bacterial infection has been extensively investigated; however, little is known about how bacterial pathogens timely shut down infecting machinery after successful infections. Here, a previously unknown sucrose–SghR/SghA–SAG–SA signaling axis was identified which controls the timing to shut off bacterial virulence expression and fine-tune host immune response. Sucrose, salicylic acid (SA), and its storage form SAG are small chemicals produced in plants whereas SghR is a bacterial sensor of sucrose and SghA is a bacterial enzyme that releases SA from SAG. Given that SA is an imperative signaling molecule in defense against a variety of microbial pathogens, these results depict a previously unknown 2-way chemical signaling cross-talk during microbe–host coevolution and shed mechanistic insights into host–bacteria interaction.
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. 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. 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 , 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 genes and are differentially transcribed at early and later infection stages, respectively. Plant metabolite sucrose is a signal ligand that inactivates SghR and consequently induces expression. Disruption of leads to increased expression and enhances tumor formation whereas mutation of decreases expression and tumor formation. These results depict a remarkable mechanism by which taps on the reserved pool of plant signal SA to reprogram its virulence upon establishment of infection. 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. 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.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. |
| Author | Chen, Shaohua Liu, Xiaoling Ye, Fuzhou Zhang, Lian-Hui Wang, Chao Yan, Xin-Fu Wang, Jianhe Wang, Jinpei Fu, Qinqin Gao, Yong-Gui Zhou, Jianuan Chang, Changqing |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31604827$$D View this record in MEDLINE/PubMed |
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| Keywords | Agrobacterium glucosidase cost–pathogen interaction sucrose chemical signaling |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 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. |
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| Snippet | It is highly intriguing how bacterial pathogens can quickly shut down energy-costly infection machinery once successful infection is established. This study... Bacterial infection has been extensively investigated; however, little is known about how bacterial pathogens timely shut down infecting machinery after... |
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| SubjectTerms | 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 |
| Title | Agrobacteria reprogram virulence gene expression by controlled release of host-conjugated signals |
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