TY - JOUR
T1 - A Plant Pathogen Type III Effector Protein Subverts Translational Regulation to Boost Host Polyamine Levels
AU - Wu, Dousheng
AU - von Roepenack-Lahaye, Edda
AU - Buntru, Matthias
AU - de Lange, Orlando
AU - Schandry, Niklas
AU - Pérez-Quintero, Alvaro L.
AU - Weinberg, Zasha
AU - Lowe-Power, Tiffany M.
AU - Szurek, Boris
AU - Michael, Anthony J.
AU - Allen, Caitilyn
AU - Schillberg, Stefan
AU - Lahaye, Thomas
N1 - Funding Information:
We thank the Lahaye Group, especially Robert Morbitzer and Annett Strauß, for their technical support and constructive suggestions. We also would like to thank Stephane Genin and Nemo Peeters for providing us with R. solanacearum strains and useful advice on how to work with them, Andreas Wachter for discussion on the RNA secondary structure prediction and helpful comments on the manuscript, Axel Strauss and Chang Liu for help on statistical analysis and figure preparation, Caterina Brancato for help on tomato transformation, and the ZMBP gardeners Johanna Schröter and Sofia Riegger for handling tomato plants. We thank Eric Kemen, Diana Horvath, Erin Ritchie, and Danalyn Holmes for helpful comments on an earlier version of this manuscript. This work was supported by grants from Deutsche Forschungsgemeinschaft (DFG) to T.L. ( LA1338/6-1 and LA1338/11-1 ).
Funding Information:
We thank the Lahaye Group, especially Robert Morbitzer and Annett Strau?, for their technical support and constructive suggestions. We also would like to thank Stephane Genin and Nemo Peeters for providing us with R. solanacearum strains and useful advice on how to work with them, Andreas Wachter for discussion on the RNA secondary structure prediction and helpful comments on the manuscript, Axel Strauss and Chang Liu for help on statistical analysis and figure preparation, Caterina Brancato for help on tomato transformation, and the ZMBP gardeners Johanna Schr?ter and Sofia Riegger for handling tomato plants. We thank Eric Kemen, Diana Horvath, Erin Ritchie, and Danalyn Holmes for helpful comments on an earlier version of this manuscript. This work was supported by grants from Deutsche Forschungsgemeinschaft (DFG) to T.L. (LA1338/6-1 and LA1338/11-1). D.W. and T.L. conceived, designed, and coordinated the study. E.v.R.-L. performed the ADC activity and metabolic assays. O.L. and N.S. initiated the project and provided preliminary material and data. M.B. performed the in vitro transcription-translation experiment under the supervision of S.S. A.P. carried out the EBE prediction under the supervision of B.S. Z.W. performed the RNA secondary structure prediction. T.M.L.-P. provided the SlADC CDS CRISPR vectors. D.W. performed all other experiments. C.A. provided helpful comments on the impact of putrescine on R. solanacearum. A.J.M. provided helpful comments on polyamine and translational regulation of ADC transcripts. D.W. and T.L. wrote the manuscript with input from all co-authors. The authors declare no competing interests.
Publisher Copyright:
© 2019 Elsevier Inc.
PY - 2019/11/13
Y1 - 2019/11/13
N2 - Pathogenic bacteria inject effector proteins into host cells to manipulate cellular processes and facilitate the infection. Transcription-activator-like effectors (TALEs), an effector class in plant pathogenic bacteria, transcriptionally activate host genes to promote disease. We identify arginine decarboxylase (ADC) genes as the host targets of Brg11, a TALE-like effector from the plant pathogen Ralstonia solanacearum. Brg11 targets a 17-bp sequence that was found to be part of a conserved 50-bp motif, termed the ADC-box, upstream of ADC genes involved in polyamine biosynthesis. The transcribed ADC-box attenuates translation from native ADC mRNAs; however, Brg11 induces truncated ADC mRNAs lacking the ADC-box, thus bypassing this translational control. As a result, Brg11 induces elevated polyamine levels that trigger a defense reaction and likely inhibits bacterial niche competitors but not R. solanacearum. Our findings suggest that Brg11 may give R. solanacearum a competitive advantage and uncover a role for bacterial effectors in regulating ternary microbe-host-microbe interactions.
AB - Pathogenic bacteria inject effector proteins into host cells to manipulate cellular processes and facilitate the infection. Transcription-activator-like effectors (TALEs), an effector class in plant pathogenic bacteria, transcriptionally activate host genes to promote disease. We identify arginine decarboxylase (ADC) genes as the host targets of Brg11, a TALE-like effector from the plant pathogen Ralstonia solanacearum. Brg11 targets a 17-bp sequence that was found to be part of a conserved 50-bp motif, termed the ADC-box, upstream of ADC genes involved in polyamine biosynthesis. The transcribed ADC-box attenuates translation from native ADC mRNAs; however, Brg11 induces truncated ADC mRNAs lacking the ADC-box, thus bypassing this translational control. As a result, Brg11 induces elevated polyamine levels that trigger a defense reaction and likely inhibits bacterial niche competitors but not R. solanacearum. Our findings suggest that Brg11 may give R. solanacearum a competitive advantage and uncover a role for bacterial effectors in regulating ternary microbe-host-microbe interactions.
KW - Ralstonia solanacearum
KW - arginine decarboxylase (ADC)
KW - microbiota
KW - polyamines
KW - putrescine
KW - rhizosphere
KW - translational regulation
KW - type III effectors
KW - upstream open reading frame (uORF)
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UR - http://www.scopus.com/inward/citedby.url?scp=85074421624&partnerID=8YFLogxK
U2 - 10.1016/j.chom.2019.09.014
DO - 10.1016/j.chom.2019.09.014
M3 - Article
C2 - 31628081
AN - SCOPUS:85074421624
SN - 1931-3128
VL - 26
SP - 638-649.e5
JO - Cell Host and Microbe
JF - Cell Host and Microbe
IS - 5
ER -