The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)

K Yu; WQ Yang; B Zhao; Ling Wang; Pan Zhang; Y Ouyang; YK Chang; GZ Chen; JL Zhang; Shujie Wang; Xiao Wang; PP Wang; Wei Wang; JA Roberts; K Jiang; LAJ Mur; XB Zhang

doi:10.1111/nph.18197

The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)

K Yu, WQ Yang, B Zhao, Ling Wang, Pan Zhang, Y Ouyang, YK Chang, GZ Chen, JL Zhang, Shujie Wang, Xiao Wang, PP Wang, Wei Wang, JA Roberts, K Jiang, LAJ Mur, XB Zhang

Department of Life Sciences

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

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Abstract

Salicylic acid (SA) is a key phytohormone regulating plant immunity. Although the transcriptional regulation of SA biosynthesis has been well-studied, its post-translational regulation is largely unknown.

We report that a Kelch repeats-containing F-box (KFB) protein, SMALL AND GLOSSY LEAVES 1 (SAGL1), negatively influences SA biosynthesis in Arabidopsis thaliana by mediating the proteolytic turnover of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1), a master transcription factor that directly drives SA biosynthesis during immunity.

Loss of SAGL1 resulted in characteristic growth inhibition. Combining metabolomic, transcriptional and phenotypic analyses, we found that SAGL1 represses SA biosynthesis and SA-mediated immune activation. Genetic crosses to mutants that are deficient in SA biosynthesis blocked the SA overaccumulation in sagl1 and rescued its growth. Biochemical and proteomic analysis identified that SAGL1 interacts with SARD1 and promotes the degradation of SARD1 in a proteasome-dependent manner.

These results unravelled a critical role of KFB protein SAGL1 in maintaining SA homeostasis via controlling SARD1 stability.

Original language	English
Pages (from-to)	885-897
Number of pages	13
Journal	New Phytologist
Volume	235
Issue number	3
Early online date	28 May 2022
DOIs	https://doi.org/10.1111/nph.18197
Publication status	Published - 30 Jun 2022

Keywords

Arabidopsis thaliana
F-box protein
growth-immunity trade-off
phenylpropanoid metabolism
salicylic acid (SA)
SARD1
PIPECOLIC ACID
ISOCHORISMATE SYNTHASE
PARTIALLY REDUNDANT
DISEASE RESISTANCE
AMINO-ACID
FAMILY
ROLES
TEMPERATURE
TOLERANCE
REGULATOR

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A China-UK joint phenomics consortium to dissect the basis of crop stress resistance in the face of climate change
Doonan, J. (PI), Han, J. (Researcher), Liu, Y. (CoI) & Mur, L. (CoI)
Biotechnology and Biological Sciences Research Council
01 Jul 2018 → 31 Dec 2023
Project: Externally funded research

Liquid Chromatography Mass Spectrometer [Q Exactive Plus]
Darby, R. (Manager)
Department of Life Sciences
Facility/equipment: Equipment

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Yu, K., Yang, WQ., Zhao, B., Wang, L., Zhang, P., Ouyang, Y., Chang, YK., Chen, GZ., Zhang, JL., Wang, S., Wang, X., Wang, PP., Wang, W., Roberts, JA., Jiang, K., Mur, LAJ., & Zhang, XB. (2022). The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1). New Phytologist, 235(3), 885-897. https://doi.org/10.1111/nph.18197

@article{3bca7bc8202f4cb1ae1450861101f548,

title = "The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)",

abstract = "Salicylic acid (SA) is a key phytohormone regulating plant immunity. Although the transcriptional regulation of SA biosynthesis has been well-studied, its post-translational regulation is largely unknown.We report that a Kelch repeats-containing F-box (KFB) protein, SMALL AND GLOSSY LEAVES 1 (SAGL1), negatively influences SA biosynthesis in Arabidopsis thaliana by mediating the proteolytic turnover of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1), a master transcription factor that directly drives SA biosynthesis during immunity.Loss of SAGL1 resulted in characteristic growth inhibition. Combining metabolomic, transcriptional and phenotypic analyses, we found that SAGL1 represses SA biosynthesis and SA-mediated immune activation. Genetic crosses to mutants that are deficient in SA biosynthesis blocked the SA overaccumulation in sagl1 and rescued its growth. Biochemical and proteomic analysis identified that SAGL1 interacts with SARD1 and promotes the degradation of SARD1 in a proteasome-dependent manner.These results unravelled a critical role of KFB protein SAGL1 in maintaining SA homeostasis via controlling SARD1 stability.",

keywords = "Arabidopsis thaliana, F-box protein, growth-immunity trade-off, phenylpropanoid metabolism, salicylic acid (SA), SARD1, PIPECOLIC ACID, ISOCHORISMATE SYNTHASE, PARTIALLY REDUNDANT, DISEASE RESISTANCE, AMINO-ACID, FAMILY, ROLES, TEMPERATURE, TOLERANCE, REGULATOR",

author = "K Yu and WQ Yang and B Zhao and Ling Wang and Pan Zhang and Y Ouyang and YK Chang and GZ Chen and JL Zhang and Shujie Wang and Xiao Wang and PP Wang and Wei Wang and JA Roberts and K Jiang and LAJ Mur and XB Zhang",

note = "Funding Information: We thank Nottingham Stock Center for most of the T‐DNA insertion mutant seeds, Kewei Zhang (Zhejiang Normal University, China) for and mutant seeds, Mingyue Gou (Henan Agricultural University, China) for suggestions in protein detection, and Kenichi Tsuda and Xiaowei Han (Huazhong Agricultural University, China) for strains and helpful discussion. This work was supported by a grant from National Natural Science Foundation of China (grant nos. 31970323 and 32170269 to XZ), a UK Biotechnology and Biological Sciences Research Council exchange grant (grant no. BB/R02118X/1 to LAJM). Arabidopsis Arabidopsis ics1ics2 s3hs5h in‐planta Pseudomonas Funding Information: We thank Nottingham Arabidopsis Stock Center for most of the Arabidopsis T-DNA insertion mutant seeds, Kewei Zhang (Zhejiang Normal University, China) for ics1ics2 and s3hs5h mutant seeds, Mingyue Gou (Henan Agricultural University, China) for suggestions in in-planta protein detection, and Kenichi Tsuda and Xiaowei Han (Huazhong Agricultural University, China) for Pseudomonas strains and helpful discussion. This work was supported by a grant from National Natural Science Foundation of China (grant nos. 31970323 and 32170269 to XZ), a UK Biotechnology and Biological Sciences Research Council exchange grant (grant no. BB/R02118X/1 to LAJM). Publisher Copyright: {\textcopyright} 2022 The Authors. New Phytologist {\textcopyright} 2022 New Phytologist Foundation.",

year = "2022",

month = jun,

day = "30",

doi = "10.1111/nph.18197",

language = "English",

volume = "235",

pages = "885--897",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley",

number = "3",

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Yu, K, Yang, WQ, Zhao, B, Wang, L, Zhang, P, Ouyang, Y, Chang, YK, Chen, GZ, Zhang, JL, Wang, S, Wang, X, Wang, PP, Wang, W, Roberts, JA, Jiang, K, Mur, LAJ & Zhang, XB 2022, 'The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)', New Phytologist, vol. 235, no. 3, pp. 885-897. https://doi.org/10.1111/nph.18197

The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1). / Yu, K; Yang, WQ; Zhao, B et al.
In: New Phytologist, Vol. 235, No. 3, 30.06.2022, p. 885-897.

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

TY - JOUR

T1 - The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)

AU - Yu, K

AU - Yang, WQ

AU - Zhao, B

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AU - Zhang, Pan

AU - Ouyang, Y

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AU - Chen, GZ

AU - Zhang, JL

AU - Wang, Shujie

AU - Wang, Xiao

AU - Wang, PP

AU - Wang, Wei

AU - Roberts, JA

AU - Jiang, K

AU - Mur, LAJ

AU - Zhang, XB

N1 - Funding Information: We thank Nottingham Stock Center for most of the T‐DNA insertion mutant seeds, Kewei Zhang (Zhejiang Normal University, China) for and mutant seeds, Mingyue Gou (Henan Agricultural University, China) for suggestions in protein detection, and Kenichi Tsuda and Xiaowei Han (Huazhong Agricultural University, China) for strains and helpful discussion. This work was supported by a grant from National Natural Science Foundation of China (grant nos. 31970323 and 32170269 to XZ), a UK Biotechnology and Biological Sciences Research Council exchange grant (grant no. BB/R02118X/1 to LAJM). Arabidopsis Arabidopsis ics1ics2 s3hs5h in‐planta Pseudomonas Funding Information: We thank Nottingham Arabidopsis Stock Center for most of the Arabidopsis T-DNA insertion mutant seeds, Kewei Zhang (Zhejiang Normal University, China) for ics1ics2 and s3hs5h mutant seeds, Mingyue Gou (Henan Agricultural University, China) for suggestions in in-planta protein detection, and Kenichi Tsuda and Xiaowei Han (Huazhong Agricultural University, China) for Pseudomonas strains and helpful discussion. This work was supported by a grant from National Natural Science Foundation of China (grant nos. 31970323 and 32170269 to XZ), a UK Biotechnology and Biological Sciences Research Council exchange grant (grant no. BB/R02118X/1 to LAJM). Publisher Copyright: © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

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Y1 - 2022/6/30

N2 - Salicylic acid (SA) is a key phytohormone regulating plant immunity. Although the transcriptional regulation of SA biosynthesis has been well-studied, its post-translational regulation is largely unknown.We report that a Kelch repeats-containing F-box (KFB) protein, SMALL AND GLOSSY LEAVES 1 (SAGL1), negatively influences SA biosynthesis in Arabidopsis thaliana by mediating the proteolytic turnover of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1), a master transcription factor that directly drives SA biosynthesis during immunity.Loss of SAGL1 resulted in characteristic growth inhibition. Combining metabolomic, transcriptional and phenotypic analyses, we found that SAGL1 represses SA biosynthesis and SA-mediated immune activation. Genetic crosses to mutants that are deficient in SA biosynthesis blocked the SA overaccumulation in sagl1 and rescued its growth. Biochemical and proteomic analysis identified that SAGL1 interacts with SARD1 and promotes the degradation of SARD1 in a proteasome-dependent manner.These results unravelled a critical role of KFB protein SAGL1 in maintaining SA homeostasis via controlling SARD1 stability.

AB - Salicylic acid (SA) is a key phytohormone regulating plant immunity. Although the transcriptional regulation of SA biosynthesis has been well-studied, its post-translational regulation is largely unknown.We report that a Kelch repeats-containing F-box (KFB) protein, SMALL AND GLOSSY LEAVES 1 (SAGL1), negatively influences SA biosynthesis in Arabidopsis thaliana by mediating the proteolytic turnover of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1), a master transcription factor that directly drives SA biosynthesis during immunity.Loss of SAGL1 resulted in characteristic growth inhibition. Combining metabolomic, transcriptional and phenotypic analyses, we found that SAGL1 represses SA biosynthesis and SA-mediated immune activation. Genetic crosses to mutants that are deficient in SA biosynthesis blocked the SA overaccumulation in sagl1 and rescued its growth. Biochemical and proteomic analysis identified that SAGL1 interacts with SARD1 and promotes the degradation of SARD1 in a proteasome-dependent manner.These results unravelled a critical role of KFB protein SAGL1 in maintaining SA homeostasis via controlling SARD1 stability.

KW - Arabidopsis thaliana

KW - F-box protein

KW - growth-immunity trade-off

KW - phenylpropanoid metabolism

KW - salicylic acid (SA)

KW - SARD1

KW - PIPECOLIC ACID

KW - ISOCHORISMATE SYNTHASE

KW - PARTIALLY REDUNDANT

KW - DISEASE RESISTANCE

KW - AMINO-ACID

KW - FAMILY

KW - ROLES

KW - TEMPERATURE

KW - TOLERANCE

KW - REGULATOR

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U2 - 10.1111/nph.18197

DO - 10.1111/nph.18197

M3 - Article

C2 - 35491444

SN - 0028-646X

VL - 235

SP - 885

EP - 897

JO - New Phytologist

JF - New Phytologist

IS - 3

ER -

Yu K, Yang WQ, Zhao B, Wang L, Zhang P, Ouyang Y et al. The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1). New Phytologist. 2022 Jun 30;235(3):885-897. Epub 2022 May 28. doi: 10.1111/nph.18197

The Kelch-F-box protein SMALL AND GLOSSY LEAVES 1 (SAGL1) negatively influences salicylic acid biosynthesis in Arabidopsis thaliana by promoting the turn-over of transcription factor SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1)

Abstract

Keywords

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Projects

A China-UK joint phenomics consortium to dissect the basis of crop stress resistance in the face of climate change

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Liquid Chromatography Mass Spectrometer [Q Exactive Plus]

Cite this