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Title: Arabidopsis SnRK1 negatively regulates phenylpropanoid metabolism via Kelch domain-containing F-box proteins

Abstract

Phenylpropanoid metabolism represents a substantial metabolic sink for the photosynthetically fixed carbon. The evolutionarily conserved Sucrose Non-Fermenting Related Kinase 1 (SnRK1) is a major metabolic sensor that reprograms metabolism upon carbon deprivation. However, it is not clear if and how SnRK1-mediated sugar signaling pathway controls phenylpropanoid metabolism. Here, we show that Arabidopsis SnRK1 negatively regulates phenylpropanoid biosynthesis via a group of Kelch domain-containing F-Box (KFB) proteins that are responsible for the ubiquitination and degradation of phenylalanine ammonia lyase (PAL). Down-regulation of AtSnRK1 significantly promoted the accumulation of soluble phenolics and lignin polymers and drastically increased PAL cellular accumulation but only slightly altered its transcription level. Co-expression of SnRK1α with PAL in Nicotiana benthamiana leaves resulted in the severe attenuation of the latter's protein level, but protein interaction assays suggested PAL is not a direct substrate of SnRK1. Furthermore, up- or down-regulation of AtSnRK1 positively affected KFB PALs gene expression, and energy starvation upregulated KFBPAL expression, which partially depends on AtSnRK1. Collectively, our study reveals that SnRK1 negatively regulates phenylpropanoid biosynthesis, and KFBPALs act as regulatory components of the SnRK1 signaling network, transcriptionally regulated by SnRK1 and subsequently mediating proteasomal degradation of PAL in response to the cellular carbon availability.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [2]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States); Tsinghua Univ., Beijing (China)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Tsinghua Univ., Beijing (China)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1763342
Report Number(s):
BNL-220934-2021-JAAM
Journal ID: ISSN 0028-646X
Grant/Contract Number:  
SC0012704
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 229; Journal Issue: 6; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Phenylpropanoids; Kelch; repeat; domaining; containing; F-box protein; Sucrose; Non-Fermenting; Related Kinase 1; Phenylalanine; ammonia; lyase; Energy; starvation; Arabidopsis

Citation Formats

Wang, Bin, Zhao, Xianhai, Zhao, Yunjun, Shanklin, John, Zhao, Qiao, and Liu, Chang‐Jun. Arabidopsis SnRK1 negatively regulates phenylpropanoid metabolism via Kelch domain-containing F-box proteins. United States: N. p., 2020. Web. doi:10.1111/nph.17121.
Wang, Bin, Zhao, Xianhai, Zhao, Yunjun, Shanklin, John, Zhao, Qiao, & Liu, Chang‐Jun. Arabidopsis SnRK1 negatively regulates phenylpropanoid metabolism via Kelch domain-containing F-box proteins. United States. https://doi.org/10.1111/nph.17121
Wang, Bin, Zhao, Xianhai, Zhao, Yunjun, Shanklin, John, Zhao, Qiao, and Liu, Chang‐Jun. Mon . "Arabidopsis SnRK1 negatively regulates phenylpropanoid metabolism via Kelch domain-containing F-box proteins". United States. https://doi.org/10.1111/nph.17121. https://www.osti.gov/servlets/purl/1763342.
@article{osti_1763342,
title = {Arabidopsis SnRK1 negatively regulates phenylpropanoid metabolism via Kelch domain-containing F-box proteins},
author = {Wang, Bin and Zhao, Xianhai and Zhao, Yunjun and Shanklin, John and Zhao, Qiao and Liu, Chang‐Jun},
abstractNote = {Phenylpropanoid metabolism represents a substantial metabolic sink for the photosynthetically fixed carbon. The evolutionarily conserved Sucrose Non-Fermenting Related Kinase 1 (SnRK1) is a major metabolic sensor that reprograms metabolism upon carbon deprivation. However, it is not clear if and how SnRK1-mediated sugar signaling pathway controls phenylpropanoid metabolism. Here, we show that Arabidopsis SnRK1 negatively regulates phenylpropanoid biosynthesis via a group of Kelch domain-containing F-Box (KFB) proteins that are responsible for the ubiquitination and degradation of phenylalanine ammonia lyase (PAL). Down-regulation of AtSnRK1 significantly promoted the accumulation of soluble phenolics and lignin polymers and drastically increased PAL cellular accumulation but only slightly altered its transcription level. Co-expression of SnRK1α with PAL in Nicotiana benthamiana leaves resulted in the severe attenuation of the latter's protein level, but protein interaction assays suggested PAL is not a direct substrate of SnRK1. Furthermore, up- or down-regulation of AtSnRK1 positively affected KFB PALs gene expression, and energy starvation upregulated KFBPAL expression, which partially depends on AtSnRK1. Collectively, our study reveals that SnRK1 negatively regulates phenylpropanoid biosynthesis, and KFBPALs act as regulatory components of the SnRK1 signaling network, transcriptionally regulated by SnRK1 and subsequently mediating proteasomal degradation of PAL in response to the cellular carbon availability.},
doi = {10.1111/nph.17121},
journal = {New Phytologist},
number = 6,
volume = 229,
place = {United States},
year = {Mon Nov 30 00:00:00 EST 2020},
month = {Mon Nov 30 00:00:00 EST 2020}
}

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