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:
-
- Brookhaven National Lab. (BNL), Upton, NY (United States); Tsinghua Univ., Beijing (China)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- 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}
}
Works referenced in this record:
Molecular identification of phenylalanine ammonia-lyase as a substrate of a specific constitutively active Arabidopsis CDPK expressed in maize protoplasts
journal, August 2001
- Cheng, Shu-Hua; Sheen, Jen; Gerrish, Chris
- FEBS Letters, Vol. 503, Issue 2-3
Down-Regulation of Kelch Domain-Containing F-Box Protein in Arabidopsis Enhances the Production of (Poly)phenols and Tolerance to Ultraviolet Radiation
journal, December 2014
- Zhang, Xuebin; Gou, Mingyue; Guo, Chunrong
- Plant Physiology, Vol. 167, Issue 2
New GATEWAY vectors for High Throughput Analyses of Protein–Protein Interactions by Bimolecular Fluorescence Complementation
journal, September 2009
- Gehl, Christian; Waadt, Rainer; Kudla, Jörg
- Molecular Plant, Vol. 2, Issue 5
Light, the circadian clock, and sugar perception in the control of lignin biosynthesis
journal, May 2005
- Rogers, Louisa A.; Dubos, Christian; Cullis, Ian F.
- Journal of Experimental Botany, Vol. 56, Issue 416
The metabolic sensor AKIN10 modulates the Arabidopsis circadian clock in a light-dependent manner : AKIN10 in the clock
journal, March 2017
- Shin, Jieun; Sánchez-Villarreal, Alfredo; Davis, Amanda M.
- Plant, Cell & Environment, Vol. 40, Issue 7
Evidence that the Arabidopsis thaliana 3-hydroxy-3-methylglutaryl-CoA reductase 1 is phosphorylated at Ser577 in planta
journal, January 2018
- Robertlee, Jekson; Kobayashi, Keiko; Tang, Jianwei
- Plant Biotechnology, Vol. 35, Issue 1
Characterization of Flavonol Synthase and Leucoanthocyanidin Dioxygenase Genes in Arabidopsis (Further Evidence for Differential Regulation of "Early" and "Late" Genes)
journal, April 1997
- Pelletier, M. K.; Murrell, J. R.; Shirley, B. W.
- Plant Physiology, Vol. 113, Issue 4
The phenylpropanoid pathway and plant defence-a genomics perspective
journal, September 2002
- Dixon, Richard A.; Achnine, Lahoucine; Kota, Parvathi
- Molecular Plant Pathology, Vol. 3, Issue 5
Transcriptional regulation of secondary growth in Arabidopsis thaliana
journal, December 2003
- Oh, Sookyung; Park, Sunchung; Han, Kyung-Hwan
- Journal of Experimental Botany, Vol. 54, Issue 393
Functional Properties of a Phenylalanine Ammonia-Lyase Promoter from Arabidopsis
journal, September 1990
- Ohl, Stephan; Hedrick, Susan A.; Chory, Joanne
- The Plant Cell, Vol. 2, Issue 9
Cytochrome b 5 Is an Obligate Electron Shuttle Protein for Syringyl Lignin Biosynthesis in Arabidopsis
journal, April 2019
- Gou, Mingyue; Yang, Xiaoman; Zhao, Yunjun
- The Plant Cell, Vol. 31, Issue 6
Lignin and Biomass: A Negative Correlation for Wood Formation and Lignin Content in Trees
journal, October 2010
- Novaes, Evandro; Kirst, Matias; Chiang, Vincent
- Plant Physiology, Vol. 154, Issue 2
A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose
journal, August 2016
- Figueroa, Carlos M.; Lunn, John E.
- Plant Physiology, Vol. 172, Issue 1
Energy Signaling in the Regulation of Gene Expression during Stress
journal, March 2010
- Baena-González, Elena
- Molecular Plant, Vol. 3, Issue 2
Multifaceted Regulations of Gateway Enzyme Phenylalanine Ammonia-Lyase in the Biosynthesis of Phenylpropanoids
journal, January 2015
- Zhang, Xuebin; Liu, Chang-Jun
- Molecular Plant, Vol. 8, Issue 1
Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development
journal, January 2008
- Covington, Michael F.; Maloof, Julin N.; Straume, Marty
- Genome Biology, Vol. 9, Issue 8
Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase
journal, January 2003
- Halford, N. G.; Hey, S.; Jhurreea, D.
- Journal of Experimental Botany, Vol. 54, Issue 382
Snf1-RELATED KINASE1-Controlled C/S 1 -bZIP Signaling Activates Alternative Mitochondrial Metabolic Pathways to Ensure Plant Survival in Extended Darkness
journal, January 2018
- Pedrotti, Lorenzo; Weiste, Christoph; Nägele, Thomas
- The Plant Cell, Vol. 30, Issue 2
Phosphorylation of WRINKLED1 by KIN10 Results in Its Proteasomal Degradation, Providing a Link between Energy Homeostasis and Lipid Biosynthesis
journal, March 2017
- Zhai, Zhiyang; Liu, Hui; Shanklin, John
- The Plant Cell, Vol. 29, Issue 4
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Convergent energy and stress signaling
journal, September 2008
- Baena-González, Elena; Sheen, Jen
- Trends in Plant Science, Vol. 13, Issue 9
AKIN10, a representative Arabidopsis SNF1-related protein kinase 1 (SnRK1), phosphorylates and downregulates plant HMG-CoA reductase
journal, April 2017
- Robertlee, Jekson; Kobayashi, Keiko; Suzuki, Masashi
- FEBS Letters, Vol. 591, Issue 8
Regulation of Sucrose non-Fermenting Related Kinase 1 genes in Arabidopsis thaliana
journal, July 2014
- Williams, Sarah P.; Rangarajan, Padma; Donahue, Janet L.
- Frontiers in Plant Science, Vol. 5
The Acetyl Bromide Method Is Faster, Simpler and Presents Best Recovery of Lignin in Different Herbaceous Tissues than Klason and Thioglycolic Acid Methods
journal, October 2014
- Moreira-Vilar, Flavia Carolina; Siqueira-Soares, Rita de Cássia; Finger-Teixeira, Aline
- PLoS ONE, Vol. 9, Issue 10
Trehalose 6-Phosphate Positively Regulates Fatty Acid Synthesis by Stabilizing WRINKLED1
journal, September 2018
- Zhai, Zhiyang; Keereetaweep, Jantana; Liu, Hui
- The Plant Cell, Vol. 30, Issue 10
The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms
journal, June 2004
- Cochrane, Fiona C.; Davin, Laurence B.; Lewis, Norman G.
- Phytochemistry, Vol. 65, Issue 11
Phosphorylation of phenylalanine ammonia-lyase: evidence for a novel protein kinase and identification of the phosphorylated residue
journal, August 1999
- Allwood, Ellen G.; Davies, Dewi R.; Gerrish, Chris
- FEBS Letters, Vol. 457, Issue 1
Genome-Wide Characterization of the Lignification Toolbox in Arabidopsis
journal, November 2003
- Raes, Jeroen; Rohde, Antje; Christensen, Jørgen Holst
- Plant Physiology, Vol. 133, Issue 3
Arabidopsis Kelch Repeat F-Box Proteins Regulate Phenylpropanoid Biosynthesis via Controlling the Turnover of Phenylalanine Ammonia-Lyase
journal, December 2013
- Zhang, Xuebin; Gou, Mingyue; Liu, Chang-Jun
- The Plant Cell, Vol. 25, Issue 12
miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
journal, January 2013
- Confraria, Ana; Martinho, Cláudia; Elias, Alexandre
- Frontiers in Plant Science, Vol. 4
Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis
journal, December 2005
- Solfanelli, Cinzia; Poggi, Alessandra; Loreti, Elena
- Plant Physiology, Vol. 140, Issue 2
A Proteolytic Regulator Controlling Chalcone Synthase Stability and Flavonoid Biosynthesis in Arabidopsis
journal, April 2017
- Zhang, Xuebin; Abrahan, Carolina; Colquhoun, Thomas A.
- The Plant Cell, Vol. 29, Issue 5
Cloning of the SNG1 Gene of Arabidopsis Reveals a Role for a Serine Carboxypeptidase-like Protein as an Acyltransferase in Secondary Metabolism
journal, August 2000
- Lehfeldt, Claus; Shirley, Amber M.; Meyer, Knut
- The Plant Cell, Vol. 12, Issue 8
Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings: Dynamics of transcriptional and metabolic responses to sucrose
journal, January 2007
- Osuna, Daniel; Usadel, Bjorn; Morcuende, Rosa
- The Plant Journal, Vol. 49, Issue 3
Nitrogen Metabolism in Lignifying Pinus taeda Cell Cultures
journal, May 1996
- van Heerden, Pieter S.; Towers, G. H. Neil; Lewis, Norman G.
- Journal of Biological Chemistry, Vol. 271, Issue 21
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
Differential expression of four Arabidopsis PAL genes; PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis
journal, September 2008
- Olsen, Kristine M.; Lea, Unni S.; Slimestad, Rune
- Journal of Plant Physiology, Vol. 165, Issue 14
A central integrator of transcription networks in plant stress and energy signalling
journal, August 2007
- Baena-González, Elena; Rolland, Filip; Thevelein, Johan M.
- Nature, Vol. 448, Issue 7156
Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings
journal, March 2008
- Gonzalez, Antonio; Zhao, Mingzhe; Leavitt, John M.
- The Plant Journal, Vol. 53, Issue 5
Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation
journal, August 2017
- Zhai, Zhiyang; Liu, Hui; Xu, Changcheng
- Plant Physiology, Vol. 175, Issue 2
The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function
journal, November 2016
- Broeckx, Tom; Hulsmans, Sander; Rolland, Filip
- Journal of Experimental Botany, Vol. 67, Issue 22
Characterization and primary functional analysis of phenylalanine ammonia-lyase gene from Phyllostachys edulis
journal, May 2012
- Gao, Z. M.; Wang, X. C.; Peng, Z. H.
- Plant Cell Reports, Vol. 31, Issue 7
Molecular Phenotyping of the pal1 and pal2 Mutants of Arabidopsis thaliana Reveals Far-Reaching Consequences on Phenylpropanoid, Amino Acid, and Carbohydrate Metabolism
journal, September 2004
- Rohde, Antje; Morreel, Kris; Ralph, John
- The Plant Cell, Vol. 16, Issue 10
Diacylglycerol acyltransferase 1 is activated by phosphatidate and inhibited by SnRK1-catalyzed phosphorylation
journal, August 2018
- Caldo, Kristian Mark P.; Shen, Wei; Xu, Yang
- The Plant Journal, Vol. 96, Issue 2
SnRK1 activation, signaling, and networking for energy homeostasis
journal, October 2019
- Crepin, Nathalie; Rolland, Filip
- Current Opinion in Plant Biology, Vol. 51
SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants
journal, August 2015
- Mair, Andrea; Pedrotti, Lorenzo; Wurzinger, Bernhard
- eLife, Vol. 4
Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis
journal, January 2009
- Favory, Jean-Jacques; Stec, Agnieszka; Gruber, Henriette
- The EMBO Journal, Vol. 28, Issue 5