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Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato

Nucleotide binding site leucine-rich repeat (NLR) proteins of the plant innate immune system are negatively regulated by the miR482/2118 family miRNAs that are in a distinct 22-nt class of miRNAs with a double mode of action. First, they cleave the target RNA, as with the canonical 21-nt miRNAs, and...

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Autores principales: Canto-Pastor, Alex, Santos, Bruno A. M. C., Valli, Adrian A., Summers, William, Schornack, Sebastian, Baulcombe, David C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377479/
https://www.ncbi.nlm.nih.gov/pubmed/30679269
http://dx.doi.org/10.1073/pnas.1814380116
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author Canto-Pastor, Alex
Santos, Bruno A. M. C.
Valli, Adrian A.
Summers, William
Schornack, Sebastian
Baulcombe, David C.
author_facet Canto-Pastor, Alex
Santos, Bruno A. M. C.
Valli, Adrian A.
Summers, William
Schornack, Sebastian
Baulcombe, David C.
author_sort Canto-Pastor, Alex
collection PubMed
description Nucleotide binding site leucine-rich repeat (NLR) proteins of the plant innate immune system are negatively regulated by the miR482/2118 family miRNAs that are in a distinct 22-nt class of miRNAs with a double mode of action. First, they cleave the target RNA, as with the canonical 21-nt miRNAs, and second, they trigger secondary siRNA production using the target RNA as a template. Here, we address the extent to which the miR482/2118 family affects expression of NLR mRNAs and disease resistance. We show that structural differences of miR482/2118 family members in tomato (Solanum lycopersicum) are functionally significant. The predicted target of the miR482 subfamily is a conserved motif in multiple NLR mRNAs, whereas for miR2118b, it is a noncoding RNA target formed by rearrangement of several different NLR genes. From RNA sequencing and degradome data in lines expressing short tandem target mimic (STTM) RNAs of miR482/2118, we confirm the different targets of these miRNAs. The effect on NLR mRNA accumulation is slight, but nevertheless, the tomato STTM lines display enhanced resistance to infection with the oomycete and bacterial pathogens. These data implicate an RNA cascade of miRNAs and secondary siRNAs in the regulation of NLR RNAs and show that the encoded NLR proteins have a role in quantitative disease resistance in addition to dominant gene resistance that has been well characterized elsewhere. We also illustrate the use of STTM RNA in a biotechnological approach for enhancing quantitative disease resistance in highly bred cultivars.
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spelling pubmed-63774792019-02-19 Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato Canto-Pastor, Alex Santos, Bruno A. M. C. Valli, Adrian A. Summers, William Schornack, Sebastian Baulcombe, David C. Proc Natl Acad Sci U S A Biological Sciences Nucleotide binding site leucine-rich repeat (NLR) proteins of the plant innate immune system are negatively regulated by the miR482/2118 family miRNAs that are in a distinct 22-nt class of miRNAs with a double mode of action. First, they cleave the target RNA, as with the canonical 21-nt miRNAs, and second, they trigger secondary siRNA production using the target RNA as a template. Here, we address the extent to which the miR482/2118 family affects expression of NLR mRNAs and disease resistance. We show that structural differences of miR482/2118 family members in tomato (Solanum lycopersicum) are functionally significant. The predicted target of the miR482 subfamily is a conserved motif in multiple NLR mRNAs, whereas for miR2118b, it is a noncoding RNA target formed by rearrangement of several different NLR genes. From RNA sequencing and degradome data in lines expressing short tandem target mimic (STTM) RNAs of miR482/2118, we confirm the different targets of these miRNAs. The effect on NLR mRNA accumulation is slight, but nevertheless, the tomato STTM lines display enhanced resistance to infection with the oomycete and bacterial pathogens. These data implicate an RNA cascade of miRNAs and secondary siRNAs in the regulation of NLR RNAs and show that the encoded NLR proteins have a role in quantitative disease resistance in addition to dominant gene resistance that has been well characterized elsewhere. We also illustrate the use of STTM RNA in a biotechnological approach for enhancing quantitative disease resistance in highly bred cultivars. National Academy of Sciences 2019-02-12 2019-01-24 /pmc/articles/PMC6377479/ /pubmed/30679269 http://dx.doi.org/10.1073/pnas.1814380116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Canto-Pastor, Alex
Santos, Bruno A. M. C.
Valli, Adrian A.
Summers, William
Schornack, Sebastian
Baulcombe, David C.
Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title_full Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title_fullStr Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title_full_unstemmed Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title_short Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
title_sort enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic rnas in tomato
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377479/
https://www.ncbi.nlm.nih.gov/pubmed/30679269
http://dx.doi.org/10.1073/pnas.1814380116
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