Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses

Mika Nomoto; Michael Skelly; Tomotaka Itaya; Tsuyoshi Mori; Takamasa Suzuki; Tomonao Matsushita; Mutsutomo Tokizawa; Keiko Kuwata; Hitoshi Mori; Yoshiharu Y Yamamoto; Tetsuya Higashiyama; Hironaka Tsukagoshi; Yasuomi Tada; Steven H Spoel

doi:10.1016/j.celrep.2021.110125

Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses

Mika Nomoto, Michael Skelly, Tomotaka Itaya, Tsuyoshi Mori, Takamasa Suzuki, Tomonao Matsushita, Mutsutomo Tokizawa, Keiko Kuwata, Hitoshi Mori, Yoshiharu Y Yamamoto, Tetsuya Higashiyama, Hironaka Tsukagoshi, Yasuomi Tada, Steven H Spoel

School of Biological Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Plants tailor immune responses to defend against pathogens with different lifestyles. In this process antagonism between the immune hormones salicylic acid (SA) and jasmonic acid (JA)optimizes transcriptional signatures specifically to the attacker encountered. Antagonism is controlled by the transcription cofactor NPR1.The indispensable role of NPR1 in activating SA-responsive genes is well understood, but how it functions as are press or of JA-responsive genes remains unclear. Here we demonstrate that SA-induced NPR1 is recruited to JA-responsive promoter regions that are co-occupied by a JA-induced transcription complex consisting ofMYC2activatorandMED25Mediator subunit. In presence of SA, NPR1physically associatedwithJA-inducedMYC2 and inhibited transcriptional activation by disrupting its interaction with MED25.Importantly,NPR1-mediated inhibition of MYC2 was a major immune mechanism for suppressing pathogen virulence. Thus, NPR1 orchestrates the immune transcriptome not only by activating SA-responsive genes but also by acting as a corepressor of JA-responsive MYC2.

Original language	English
Article number	110125
Number of pages	34
Journal	Cell Reports
Volume	37
Issue number	11
DOIs	https://doi.org/10.1016/j.celrep.2021.110125
Publication status	Published - 14 Dec 2021

Keywords

plant immunity
salicylic acid
jasmonic acid
coronatine
biotroph
necrotroph
pseudomonas syringae
NPR1
MYC2
MED25

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10.1016/j.celrep.2021.110125Licence: Creative Commons: Attribution-NonCommercial-NoDerivatives (CC BY-NC-ND)

TadaEtalCR2021SuppressionOfMYCTranscriptionActivatorsByTheImmuneCofactorNPR1Final published version, 3.22 MBLicence: Creative Commons: Attribution-NonCommercial-NoDerivatives (CC BY-NC-ND)

Cellular Functions of Proteasome-Associated Ubiquitin Ligase Activity
Spoel, S. & Bayne, E.
BBSRC
1/12/19 → 1/04/23
Project: Research
Understanding the influence of environmental signals on establishment of plant disease resistance
Spoel, S.
UK-based charities
16/03/18 → 15/03/20
Project: Research
IMMUNE-EXPRESS: Proteasome-Mediated Gene Expression in Plant Immunity
Spoel, S.
EU government bodies
1/03/16 → 31/08/21
Project: Research

Cite this

Nomoto, M., Skelly, M., Itaya, T., Mori, T., Suzuki, T., Matsushita, T., Tokizawa, M., Kuwata, K., Mori, H., Yamamoto, Y. Y., Higashiyama, T., Tsukagoshi, H., Tada, Y., & Spoel, S. H. (2021). Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses. Cell Reports, 37(11), [110125]. https://doi.org/10.1016/j.celrep.2021.110125

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title = "Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses",

abstract = "Plants tailor immune responses to defend against pathogens with different lifestyles. In this process antagonism between the immune hormones salicylic acid (SA) and jasmonic acid (JA)optimizes transcriptional signatures specifically to the attacker encountered. Antagonism is controlled by the transcription cofactor NPR1.The indispensable role of NPR1 in activating SA-responsive genes is well understood, but how it functions as are press or of JA-responsive genes remains unclear. Here we demonstrate that SA-induced NPR1 is recruited to JA-responsive promoter regions that are co-occupied by a JA-induced transcription complex consisting ofMYC2activatorandMED25Mediator subunit. In presence of SA, NPR1physically associatedwithJA-inducedMYC2 and inhibited transcriptional activation by disrupting its interaction with MED25.Importantly,NPR1-mediated inhibition of MYC2 was a major immune mechanism for suppressing pathogen virulence. Thus, NPR1 orchestrates the immune transcriptome not only by activating SA-responsive genes but also by acting as a corepressor of JA-responsive MYC2.",

keywords = "plant immunity, salicylic acid, jasmonic acid, coronatine, biotroph, necrotroph, pseudomonas syringae, NPR1, MYC2, MED25",

author = "Mika Nomoto and Michael Skelly and Tomotaka Itaya and Tsuyoshi Mori and Takamasa Suzuki and Tomonao Matsushita and Mutsutomo Tokizawa and Keiko Kuwata and Hitoshi Mori and Yamamoto, {Yoshiharu Y} and Tetsuya Higashiyama and Hironaka Tsukagoshi and Yasuomi Tada and Spoel, {Steven H}",

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doi = "10.1016/j.celrep.2021.110125",

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volume = "37",

journal = "Cell Reports",

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T1 - Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses

AU - Nomoto, Mika

AU - Skelly, Michael

AU - Itaya, Tomotaka

AU - Mori, Tsuyoshi

AU - Suzuki, Takamasa

AU - Matsushita, Tomonao

AU - Tokizawa, Mutsutomo

AU - Kuwata, Keiko

AU - Mori, Hitoshi

AU - Yamamoto, Yoshiharu Y

AU - Higashiyama, Tetsuya

AU - Tsukagoshi, Hironaka

AU - Tada, Yasuomi

AU - Spoel, Steven H

PY - 2021/12/14

Y1 - 2021/12/14

N2 - Plants tailor immune responses to defend against pathogens with different lifestyles. In this process antagonism between the immune hormones salicylic acid (SA) and jasmonic acid (JA)optimizes transcriptional signatures specifically to the attacker encountered. Antagonism is controlled by the transcription cofactor NPR1.The indispensable role of NPR1 in activating SA-responsive genes is well understood, but how it functions as are press or of JA-responsive genes remains unclear. Here we demonstrate that SA-induced NPR1 is recruited to JA-responsive promoter regions that are co-occupied by a JA-induced transcription complex consisting ofMYC2activatorandMED25Mediator subunit. In presence of SA, NPR1physically associatedwithJA-inducedMYC2 and inhibited transcriptional activation by disrupting its interaction with MED25.Importantly,NPR1-mediated inhibition of MYC2 was a major immune mechanism for suppressing pathogen virulence. Thus, NPR1 orchestrates the immune transcriptome not only by activating SA-responsive genes but also by acting as a corepressor of JA-responsive MYC2.

AB - Plants tailor immune responses to defend against pathogens with different lifestyles. In this process antagonism between the immune hormones salicylic acid (SA) and jasmonic acid (JA)optimizes transcriptional signatures specifically to the attacker encountered. Antagonism is controlled by the transcription cofactor NPR1.The indispensable role of NPR1 in activating SA-responsive genes is well understood, but how it functions as are press or of JA-responsive genes remains unclear. Here we demonstrate that SA-induced NPR1 is recruited to JA-responsive promoter regions that are co-occupied by a JA-induced transcription complex consisting ofMYC2activatorandMED25Mediator subunit. In presence of SA, NPR1physically associatedwithJA-inducedMYC2 and inhibited transcriptional activation by disrupting its interaction with MED25.Importantly,NPR1-mediated inhibition of MYC2 was a major immune mechanism for suppressing pathogen virulence. Thus, NPR1 orchestrates the immune transcriptome not only by activating SA-responsive genes but also by acting as a corepressor of JA-responsive MYC2.

KW - plant immunity

KW - salicylic acid

KW - jasmonic acid

KW - coronatine

KW - biotroph

KW - necrotroph

KW - pseudomonas syringae

KW - NPR1

KW - MYC2

KW - MED25

U2 - 10.1016/j.celrep.2021.110125

DO - 10.1016/j.celrep.2021.110125

M3 - Article

VL - 37

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 11

M1 - 110125

ER -

Suppression of MYC transcription activators by the immune cofactor NPR1 fine tunes plant immune responses

Abstract

Keywords

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Projects

Cellular Functions of Proteasome-Associated Ubiquitin Ligase Activity

Understanding the influence of environmental signals on establishment of plant disease resistance

IMMUNE-EXPRESS: Proteasome-Mediated Gene Expression in Plant Immunity

Cite this