CYCLIN‐DEPENDENT KINASE 8 positively regulates oil synthesis by activating WRINKLED1 transcription
Abstract
Summary CYCLIN‐DEPENDENT KINASE 8 (CDK8), a component of the kinase module of the Mediator complex in Arabidopsis, is involved in many processes, including flowering, plant defense, drought, and energy stress responses. Here, we investigated cdk8 mutants and CDK8‐ overexpressing lines to evaluate whether CDK8 also plays a role in regulating lipid synthesis, an energy‐demanding anabolism. Quantitative lipid analysis demonstrated significant reductions in lipid synthesis rates and lipid accumulation in developing siliques and seedlings of cdk8 , and conversely, elevated lipid contents in wild‐type seed overexpressing CDK8 . Transactivation assays show that CDK8 is necessary for maximal transactivation of the master seed oil activator WRINKLED1 (WRI1) by the seed maturation transcription factor ABSCISIC ACID INSENSITIVE3, supporting a direct regulatory role of CDK8 in oil synthesis. Thermophoretic studies show GEMINIVIRUS REP INTERACTING KINASE1, an activating kinase of KIN10 (a catalytic subunit of SUCROSE NON‐FERMENTING1‐RELATED KINASE1), physically interacts with CDK8, resulting in its phosphorylation and degradation in the presence of KIN10. This work defines a mechanism whereby, once activated, KIN10 downregulates WRI1 expression and suppresses lipid synthesis via promoting the degradation of CDK8. The KIN10‐CDK8‐dependent regulation of lipid synthesis described herein is additional to our previously reported KIN10‐dependent phosphorylation and degradation of WRI1.
- Authors:
-
- Department of Biology Brookhaven National Laboratory Building 463, 50 Bell Ave Upton NY 11973 USA
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1968373
- Alternate Identifier(s):
- OSTI ID: 1913820; OSTI ID: 1961924
- Report Number(s):
- BNL-223882-2023-JAAM
Journal ID: ISSN 0028-646X
- Grant/Contract Number:
- DE‐SC0012704; SC0012704
- Resource Type:
- Published Article
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 238 Journal Issue: 2; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; triacylgycerol(TAG); seed oil; protein kinase; CDK8; WRI1; SnRK1; KIN10; GRIK1
Citation Formats
Zhai, Zhiyang, Blanford, Jantana K., Cai, Yingqi, Sun, Jing, Liu, Hui, Shi, Hai, Schwender, Jorg, and Shanklin, John. CYCLIN‐DEPENDENT KINASE 8 positively regulates oil synthesis by activating WRINKLED1 transcription. United Kingdom: N. p., 2023.
Web. doi:10.1111/nph.18764.
Zhai, Zhiyang, Blanford, Jantana K., Cai, Yingqi, Sun, Jing, Liu, Hui, Shi, Hai, Schwender, Jorg, & Shanklin, John. CYCLIN‐DEPENDENT KINASE 8 positively regulates oil synthesis by activating WRINKLED1 transcription. United Kingdom. https://doi.org/10.1111/nph.18764
Zhai, Zhiyang, Blanford, Jantana K., Cai, Yingqi, Sun, Jing, Liu, Hui, Shi, Hai, Schwender, Jorg, and Shanklin, John. Thu .
"CYCLIN‐DEPENDENT KINASE 8 positively regulates oil synthesis by activating WRINKLED1 transcription". United Kingdom. https://doi.org/10.1111/nph.18764.
@article{osti_1968373,
title = {CYCLIN‐DEPENDENT KINASE 8 positively regulates oil synthesis by activating WRINKLED1 transcription},
author = {Zhai, Zhiyang and Blanford, Jantana K. and Cai, Yingqi and Sun, Jing and Liu, Hui and Shi, Hai and Schwender, Jorg and Shanklin, John},
abstractNote = {Summary CYCLIN‐DEPENDENT KINASE 8 (CDK8), a component of the kinase module of the Mediator complex in Arabidopsis, is involved in many processes, including flowering, plant defense, drought, and energy stress responses. Here, we investigated cdk8 mutants and CDK8‐ overexpressing lines to evaluate whether CDK8 also plays a role in regulating lipid synthesis, an energy‐demanding anabolism. Quantitative lipid analysis demonstrated significant reductions in lipid synthesis rates and lipid accumulation in developing siliques and seedlings of cdk8 , and conversely, elevated lipid contents in wild‐type seed overexpressing CDK8 . Transactivation assays show that CDK8 is necessary for maximal transactivation of the master seed oil activator WRINKLED1 (WRI1) by the seed maturation transcription factor ABSCISIC ACID INSENSITIVE3, supporting a direct regulatory role of CDK8 in oil synthesis. Thermophoretic studies show GEMINIVIRUS REP INTERACTING KINASE1, an activating kinase of KIN10 (a catalytic subunit of SUCROSE NON‐FERMENTING1‐RELATED KINASE1), physically interacts with CDK8, resulting in its phosphorylation and degradation in the presence of KIN10. This work defines a mechanism whereby, once activated, KIN10 downregulates WRI1 expression and suppresses lipid synthesis via promoting the degradation of CDK8. The KIN10‐CDK8‐dependent regulation of lipid synthesis described herein is additional to our previously reported KIN10‐dependent phosphorylation and degradation of WRI1.},
doi = {10.1111/nph.18764},
journal = {New Phytologist},
number = 2,
volume = 238,
place = {United Kingdom},
year = {Thu Feb 16 00:00:00 EST 2023},
month = {Thu Feb 16 00:00:00 EST 2023}
}
https://doi.org/10.1111/nph.18764
Works referenced in this record:
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
Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants
journal, August 2007
- Nakagawa, Tsuyoshi; Suzuki, Takamasa; Murata, Satoko
- Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 8
The Mediator Complex MED15 Subunit Mediates Activation of Downstream Lipid-Related Genes by the WRINKLED1 Transcription Factor
journal, May 2016
- Kim, Mi Jung; Jang, In-Cheol; Chua, Nam-Hai
- Plant Physiology, Vol. 171, Issue 3
AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis: Interaction between FUSCA3 and AKIN10
journal, December 2011
- Tsai, Allen Yi-Lun; Gazzarrini, Sonia
- The Plant Journal, Vol. 69, Issue 5
An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis
journal, November 2009
- Maeo, Kenichiro; Tokuda, Tsuyoshi; Ayame, Atsuko
- The Plant Journal, Vol. 60, Issue 3
The Pumilio RNA‐binding protein APUM24 regulates seed maturation by fine‐tuning the BPM‐WRI1 module in
Arabidopsis
journal, June 2021
- Huang, Ruihua; Liu, Mengling; Gong, Guanping
- Journal of Integrative Plant Biology, Vol. 63, Issue 7
Geminivirus Infection Up-Regulates the Expression of Two Arabidopsis Protein Kinases Related to Yeast SNF1- and Mammalian AMPK-Activating Kinases
journal, October 2006
- Shen, Wei; Hanley-Bowdoin, Linda
- Plant Physiology, Vol. 142, Issue 4
Arabidopsis Protein Kinases GRIK1 and GRIK2 Specifically Activate SnRK1 by Phosphorylating Its Activation Loop
journal, April 2009
- Shen, Wei; Reyes, Maria Ines; Hanley-Bowdoin, Linda
- Plant Physiology, Vol. 150, Issue 2
CYCLIN-DEPENDENT KINASE8 Differentially Regulates Plant Immunity to Fungal Pathogens through Kinase-Dependent and -Independent Functions in Arabidopsis
journal, October 2014
- Zhu, Yingfang; Schluttenhoffer, Craig M.; Wang, Pengcheng
- The Plant Cell, Vol. 26, Issue 10
WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis
journal, September 2004
- Cernac, Alex; Benning, Christoph
- The Plant Journal, Vol. 40, Issue 4, p. 575-585
CDK8 is associated with RAP2.6 and SnRK2.6 and positively modulates abscisic acid signaling and drought response inArabidopsis
journal, August 2020
- Zhu, Yingfang; Huang, Pengcheng; Guo, Pengcheng
- New Phytologist, Vol. 228, Issue 5
A kinase–cyclin pair in the RNA polymerase II holoenzyme
journal, March 1995
- Liao, Sha-Mei; Zhang, Jianhua; Jeffery, Douglas A.
- Nature, Vol. 374, Issue 6518
Expression of a Bacterial Trehalose-6-phosphate Synthase otsA Increases Oil Accumulation in Plant Seeds and Vegetative Tissues
journal, March 2021
- Zhai, Zhiyang; Keereetaweep, Jantana; Liu, Hui
- Frontiers in Plant Science, Vol. 12
Establishing RNA Interference as a Reverse-Genetic Approach for Gene Functional Analysis in Protoplasts
journal, November 2008
- Zhai, Zhiyang; Sooksa-nguan, Thanwalee; Vatamaniuk, Olena K.
- Plant Physiology, Vol. 149, Issue 2
A generic protocol for the expression and purification of recombinant proteins in Escherichia coli using a combinatorial His6-maltose binding protein fusion tag
journal, February 2007
- Nallamsetty, Sreedevi; Waugh, David S.
- Nature Protocols, Vol. 2, Issue 2
On the Export of Fatty Acids from the Chloroplast
journal, February 2004
- Koo, Abraham J. K.; Ohlrogge, John B.; Pollard, Mike
- Journal of Biological Chemistry, Vol. 279, Issue 16
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
HSI2/VAL1 Silences AGL15 to Regulate the Developmental Transition from Seed Maturation to Vegetative Growth in Arabidopsis
journal, February 2018
- Chen, Naichong; Veerappan, Vijaykumar; Abdelmageed, Haggag
- The Plant Cell, Vol. 30, Issue 3
FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells
journal, August 2016
- Zhang, Meng; Cao, Xia; Jia, Qingli
- The Plant Journal, Vol. 88, Issue 1
The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function
journal, February 2009
- Knuesel, M. T.; Meyer, K. D.; Bernecky, C.
- Genes & Development, Vol. 23, Issue 4
Characterization of Mediator Complexes from HeLa Cell Nuclear Extract
journal, July 2001
- Wang, Gang; Cantin, Greg T.; Stevens, Jennitte L.
- Molecular and Cellular Biology, Vol. 21, Issue 14
WRINKLED1, A Ubiquitous Regulator in Oil Accumulating Tissues from Arabidopsis Embryos to Oil Palm Mesocarp
journal, July 2013
- Ma, Wei; Kong, Que; Arondel, Vincent
- PLoS ONE, Vol. 8, Issue 7
WRINKLED1 Is Subject to Evolutionary Conserved Negative Autoregulation
journal, March 2019
- Snell, Per; Grimberg, Åsa; Carlsson, Anders S.
- Frontiers in Plant Science, Vol. 10
TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR4 Interacts with WRINKLED1 to Mediate Seed Oil Biosynthesis
journal, July 2020
- Kong, Que; Singh, Sanjay K.; Mantyla, Jenny J.
- Plant Physiology, Vol. 184, Issue 2
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
Purple acid phosphatase2 stimulates a futile cycle of lipid synthesis and degradation, and mitigates the negative growth effects of triacylglycerol accumulation in vegetative tissues
journal, August 2022
- Cai, Yingqi; Zhai, Zhiyang; Blanford, Jantana
- New Phytologist, Vol. 236, Issue 3
The CYCLIN-DEPENDENT KINASE Module of the Mediator Complex Promotes Flowering and Reproductive Development in Pea
journal, January 2020
- Hasan, A. S. M. Mainul; Vander Schoor, Jacqueline K.; Hecht, Valerie
- Plant Physiology, Vol. 182, Issue 3
An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development
journal, August 2022
- Kuczynski, Cathleen; McCorkle, Sean; Keereetaweep, Jantana
- Frontiers in Plant Science, Vol. 13
WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis: Oil synthesis regulatory network in seeds
journal, April 2007
- Baud, Sébastien; Mendoza, Monica Santos; To, Alexandra
- The Plant Journal, Vol. 50, Issue 5
The impact of Arabidopsis thaliana SNF 1‐related‐kinase 1 (Sn RK 1)‐activating kinase 1 (Sn AK 1) and Sn AK 2 on Sn RK 1 phosphorylation status: characterization of a Sn AK double mutant
journal, February 2017
- Glab, Nathalie; Oury, Céline; Guérinier, Thomas
- The Plant Journal, Vol. 89, Issue 5
The Transcription Corepressor LEUNIG Interacts with the Histone Deacetylase HDA19 and Mediator Components MED14 (SWP) and CDK8 (HEN3) To Repress Transcription
journal, August 2007
- Gonzalez, Deyarina; Bowen, Adam J.; Carroll, Thomas S.
- Molecular and Cellular Biology, Vol. 27, Issue 15
Analysis of Metabolic Flux Phenotypes for Two Arabidopsis Mutants with Severe Impairment in Seed Storage Lipid Synthesis
journal, September 2009
- Lonien, Joachim; Schwender, Jörg
- Plant Physiology, Vol. 151, Issue 3
Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation
journal, August 2016
- Nukarinen, Ella; Nägele, Thomas; Pedrotti, Lorenzo
- Scientific Reports, Vol. 6, Issue 1
HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis
journal, July 2004
- Wang, W.
- Development, Vol. 131, Issue 13
TFIIH is negatively regulated by cdk8-containing mediator complexes
journal, September 2000
- Akoulitchev, Sasha; Chuikov, Sergei; Reinberg, Danny
- Nature, Vol. 407, Issue 6800
ABA-INSENSITIVE 3 with or without FUSCA3 highly up-regulates lipid droplet proteins and activates oil accumulation
journal, November 2021
- Yang, Zheng; Liu, Xiangling; Wang, Kai
- Journal of Experimental Botany, Vol. 73, Issue 7
Arabidopsis BPM Proteins Function as Substrate Adaptors to a CULLIN3-Based E3 Ligase to Affect Fatty Acid Metabolism in Plants
journal, June 2013
- Chen, L.; Lee, J. H.; Weber, H.
- The Plant Cell, Vol. 25, Issue 6
Triacylglycerol biosynthesis in shaded seeds of tung tree (
Vernicia fordii
) is regulated in part by
Homeodomain Leucine Zipper 21
journal, October 2021
- Zhang, Lingling; Wu, Pan; Li, Wenying
- The Plant Journal, Vol. 108, Issue 6
Cyclin-dependent kinases: a family portrait
journal, November 2009
- Malumbres, Marcos; Harlow, Edward; Hunt, Tim
- Nature Cell Biology, Vol. 11, Issue 11
NPR1 Promotes Its Own and Target Gene Expression in Plant Defense by Recruiting CDK8
journal, May 2019
- Chen, Jian; Mohan, Rajinikanth; Zhang, Yuqiang
- Plant Physiology, Vol. 181, Issue 1
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
Gal4 turnover and transcription activation
journal, October 2009
- Collins, Galen A.; Lipford, J. Russell; Deshaies, Raymond J.
- Nature, Vol. 461, Issue 7265
Genome-Wide Analysis of Core Cell Cycle Genes in Arabidopsis
journal, April 2002
- Vandepoele, Klaas; Raes, Jeroen; De Veylder, Lieven
- The Plant Cell, Vol. 14, Issue 4
Preparation, composition and functional properties of pennycress (Thlaspi arvense L.) seed protein isolates
journal, April 2014
- Hojilla-Evangelista, Mila P.; Selling, Gordon W.; Berhow, Mark A.
- Industrial Crops and Products, Vol. 55
Sumoylation of transcription factor Gcn4 facilitates its Srb10-mediated clearance from promoters in yeast
journal, February 2012
- Rosonina, Emanuel; Duncan, Sarah M.; Manley, James L.
- Genes & Development, Vol. 26, Issue 4
Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues
journal, April 2016
- Xu, Changcheng; Shanklin, John
- Annual Review of Plant Biology, Vol. 67, Issue 1
pSITE Vectors for Stable Integration or Transient Expression of Autofluorescent Protein Fusions in Plants: Probing Nicotiana benthamiana- Virus Interactions
journal, July 2007
- Chakrabarty, Romit; Banerjee, Rituparna; Chung, Sang-Min
- Molecular Plant-Microbe Interactions®, Vol. 20, Issue 7
The AMP-Activated Protein Kinase KIN10 Is Involved in the Regulation of Autophagy in Arabidopsis
journal, July 2017
- Chen, Liang; Su, Ze-Zhuo; Huang, Li
- Frontiers in Plant Science, Vol. 8
Plasticity and innovation of regulatory mechanisms underlying seed oil content mediated by duplicated genes in the palaeopolyploid soybean
journal, April 2017
- Zhang, Dajian; Zhao, Meixia; Li, Shuai
- The Plant Journal, Vol. 90, Issue 6
A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues
journal, May 1957
- Folch, Jordi; Lees, M.; Stanley, G. H. Sloane
- Journal of Biological Chemistry, Vol. 226, Issue 1
Temporal Regulation of RNA Polymerase II by Srb10 and Kin28 Cyclin-Dependent Kinases
journal, July 1998
- Hengartner, Christoph J.; Myer, Vic E.; Liao, Sha-Mei
- Molecular Cell, Vol. 2, Issue 1
GAL4 Is Regulated by the RNA Polymerase II Holoenzyme–Associated Cyclin-Dependent Protein Kinase SRB10/CDK8
journal, May 1999
- Hirst, Martin; Kobor, Michael S.; Kuriakose, Neena
- Molecular Cell, Vol. 3, Issue 5
The Role of Sugar Signaling in Regulating Plant Fatty Acid Synthesis
journal, March 2021
- Zhai, Zhiyang; Keereetaweep, Jantana; Liu, Hui
- Frontiers in Plant Science, Vol. 12
A Complex of the Srb8, -9, -10, and -11 Transcriptional Regulatory Proteins from Yeast
journal, August 2002
- Borggrefe, Tilman; Davis, Ralph; Erdjument-Bromage, Hediye
- Journal of Biological Chemistry, Vol. 277, Issue 46
The plant lipidome in human and environmental health
journal, September 2016
- Horn, P. J.; Benning, C.
- Science, Vol. 353, Issue 6305
Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatography-tandem mass spectrometry
journal, August 2006
- Bajad, Sunil U.; Lu, Wenyun; Kimball, Elizabeth H.
- Journal of Chromatography A, Vol. 1125, Issue 1, p. 76-88
Trehalose‐6‐phosphate signaling regulates thermoresponsive hypocotyl growth in Arabidopsis thaliana
journal, August 2019
- Hwang, Geonhee; Kim, Sara; Cho, Jae‐Yong
- EMBO reports, Vol. 20, Issue 10
Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis
journal, August 2022
- Shi, Wen; Wang, Lingyan; Yao, Lianmei
- Nature Communications, Vol. 13, Issue 1
A putative stimulatory role for activator turnover in gene expression
journal, November 2005
- Lipford, J. Russell; Smith, Geoffrey T.; Chi, Yong
- Nature, Vol. 438, Issue 7064
wrinkled1 : A Novel, Low-Seed-Oil Mutant of Arabidopsis with a Deficiency in the Seed-Specific Regulation of Carbohydrate Metabolism
journal, September 1998
- Focks, Nicole; Benning, Christoph
- Plant Physiology, Vol. 118, Issue 1
Cyclin-dependent Kinase E1 (CDKE1) Provides a Cellular Switch in Plants between Growth and Stress Responses
journal, December 2012
- Ng, Sophia; Giraud, Estelle; Duncan, Owen
- Journal of Biological Chemistry, Vol. 288, Issue 5
BLISTER promotes seed maturation and fatty acid biosynthesis by interacting with WRINKLED1 to regulate chromatin dynamics in Arabidopsis
journal, March 2022
- Huang, Ruihua; Liu, Mengling; Gong, Guanping
- The Plant Cell, Vol. 34, Issue 6
Default Activation and Nuclear Translocation of the Plant Cellular Energy Sensor SnRK1 Regulate Metabolic Stress Responses and Development
journal, May 2019
- Ramon, Matthew; Dang, Tuong Vi T.; Broeckx, Tom
- The Plant Cell, Vol. 31, Issue 7