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Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity

Regulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that SRFR1, a negative regulator of effector-triggered...

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Autores principales: Garner, Christopher M., Spears, Benjamin J., Su, Jianbin, Cseke, Leland J., Smith, Samantha N., Rogan, Conner J., Gassmann, Walter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7935258/
https://www.ncbi.nlm.nih.gov/pubmed/33621240
http://dx.doi.org/10.1371/journal.pgen.1009026
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author Garner, Christopher M.
Spears, Benjamin J.
Su, Jianbin
Cseke, Leland J.
Smith, Samantha N.
Rogan, Conner J.
Gassmann, Walter
author_facet Garner, Christopher M.
Spears, Benjamin J.
Su, Jianbin
Cseke, Leland J.
Smith, Samantha N.
Rogan, Conner J.
Gassmann, Walter
author_sort Garner, Christopher M.
collection PubMed
description Regulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that SRFR1, a negative regulator of effector-triggered immunity, interacts with SNC1 and EDS1. When SRFR1 is non-functional in the Arabidopsis accession Col-0, SNC1 levels increase, causing a cascade of events that lead to autoimmunity phenotypes. Previous work showed that some members of the transcriptional co-repressor family TOPLESS interact with SNC1 to repress negative regulators of immunity. Therefore, to explore potential connections between SRFR1 and TOPLESS family members, we took a genetic approach that examined the effect of each TOPLESS member in the srfr1 mutant background. The data indicated that an additive genetic interaction exists between SRFR1 and two members of the TOPLESS family, TPR2 and TPR3, as demonstrated by increased stunting and elevated PR2 expression in srfr1 tpr2 and srfr1 tpr2 tpr3 mutants. Furthermore, the tpr2 mutation intensifies autoimmunity in the auto-active snc1-1 mutant, indicating a novel role of these TOPLESS family members in negatively regulating SNC1-dependent phenotypes. This negative regulation can also be reversed by overexpressing TPR2 in the srfr1 tpr2 background. Similar to TPR1 that positively regulates snc1-1 phenotypes by interacting with SNC1, we show here that TPR2 directly binds the N-terminal domain of SNC1. In addition, TPR2 interacts with TPR1 in vivo, suggesting that the opposite functions of TPR2 and TPR1 are based on titration of SNC1-TPR1 complexes by TPR2 or altered functions of a SNC1-TPR1-TPR2 complex. Thus, this work uncovers diverse functions of individual members of the TOPLESS family in Arabidopsis and provides evidence for the additive effect of transcriptional and post-transcriptional regulation of SNC1.
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spelling pubmed-79352582021-03-15 Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity Garner, Christopher M. Spears, Benjamin J. Su, Jianbin Cseke, Leland J. Smith, Samantha N. Rogan, Conner J. Gassmann, Walter PLoS Genet Research Article Regulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that SRFR1, a negative regulator of effector-triggered immunity, interacts with SNC1 and EDS1. When SRFR1 is non-functional in the Arabidopsis accession Col-0, SNC1 levels increase, causing a cascade of events that lead to autoimmunity phenotypes. Previous work showed that some members of the transcriptional co-repressor family TOPLESS interact with SNC1 to repress negative regulators of immunity. Therefore, to explore potential connections between SRFR1 and TOPLESS family members, we took a genetic approach that examined the effect of each TOPLESS member in the srfr1 mutant background. The data indicated that an additive genetic interaction exists between SRFR1 and two members of the TOPLESS family, TPR2 and TPR3, as demonstrated by increased stunting and elevated PR2 expression in srfr1 tpr2 and srfr1 tpr2 tpr3 mutants. Furthermore, the tpr2 mutation intensifies autoimmunity in the auto-active snc1-1 mutant, indicating a novel role of these TOPLESS family members in negatively regulating SNC1-dependent phenotypes. This negative regulation can also be reversed by overexpressing TPR2 in the srfr1 tpr2 background. Similar to TPR1 that positively regulates snc1-1 phenotypes by interacting with SNC1, we show here that TPR2 directly binds the N-terminal domain of SNC1. In addition, TPR2 interacts with TPR1 in vivo, suggesting that the opposite functions of TPR2 and TPR1 are based on titration of SNC1-TPR1 complexes by TPR2 or altered functions of a SNC1-TPR1-TPR2 complex. Thus, this work uncovers diverse functions of individual members of the TOPLESS family in Arabidopsis and provides evidence for the additive effect of transcriptional and post-transcriptional regulation of SNC1. Public Library of Science 2021-02-23 /pmc/articles/PMC7935258/ /pubmed/33621240 http://dx.doi.org/10.1371/journal.pgen.1009026 Text en © 2021 Garner et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Garner, Christopher M.
Spears, Benjamin J.
Su, Jianbin
Cseke, Leland J.
Smith, Samantha N.
Rogan, Conner J.
Gassmann, Walter
Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title_full Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title_fullStr Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title_full_unstemmed Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title_short Opposing functions of the plant TOPLESS gene family during SNC1-mediated autoimmunity
title_sort opposing functions of the plant topless gene family during snc1-mediated autoimmunity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7935258/
https://www.ncbi.nlm.nih.gov/pubmed/33621240
http://dx.doi.org/10.1371/journal.pgen.1009026
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