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Title: Phosphorylation of WRINKLED1 by KIN10 Results in its Proteasomal Degradation, Providing a Link Between Energy Homeostasis and Lipid Biosynthesis

Journal Article · · The Plant Cell
DOI:https://doi.org/10.1105/tpc.17.00019· OSTI ID:1348294

WRINKLED1 (WRI1), a member of the APETALA2 (AP2) class of transcription factors, positively regulates glycolysis and lipid biosynthesis in Arabidopsis thaliana. Here we identify mechanistic links between KIN10, the major SUCROSE NON-FERMENTATION-1 (SNF1)-RELATED KINASE 1 (SnRK1) involved in sugar/energy homeostasis and the posttranslational regulation of WRI1. Transient expression of WRI1 with OLEOSIN1 (OLE1) in Nicotiana benthamiana stimulates triacylglycerol (TAG) accumulation, but their coexpression with KIN10 abrogates this effect by inducing proteasomal degradation of WRI1. While WRI1 lacks canonical KIN10 target sequences, we demonstrated direct KIN10-dependent phosphorylation of WRI1 using purified E. coli-expressed components. The resulting phosphorylated WRI1 was more rapidly degraded than native WRI1 in cell-free degradation assays. WRI1 phosphorylation was localized to two variants of the canonical KIN10 recognition sequence, one in each of its two AP2 DNA-binding domains. Conversion of the phosphorylation sites at T70 and S166 to Ala resulted in a loss of KIN10-dependent phosphorylation, and when coexpressed with KIN10 the WRI1 double mutant accumulated to 2-3 fold higher levels than native WRI1. In conclusion, KIN10-dependent degradation of WRI1 provides a homeostatic mechanism that favors lipid biosynthesis when intracellular sugar levels are elevated and KIN10 is inhibited; conversely, glycolysis and lipid biosynthesis are curtailed as sugar levels decrease and KIN10 regains activity.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0012704
OSTI ID:
1348294
Report Number(s):
BNL-113680-2017-JA
Journal Information:
The Plant Cell, Vol. 29, Issue 4; ISSN 1040-4651
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 87 works
Citation information provided by
Web of Science

Cited By (17)

Properties and Biotechnological Applications of Acyl-CoA:diacylglycerol Acyltransferase and Phospholipid:diacylglycerol Acyltransferase from Terrestrial Plants and Microalgae journal July 2018
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WRINKLED1 as a novel 14-3-3 client: function of 14-3-3 proteins in plant lipid metabolism journal August 2018
GhHUB2, a ubiquitin ligase, is involved in cotton fiber development via the ubiquitin–26S proteasome pathway journal July 2018
The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development journal February 2019
An Apple Protein Kinase MdSnRK1.1 Interacts with MdCAIP1 to Regulate ABA Sensitivity journal July 2017
Cellular Organization and Regulation of Plant Glycerolipid Metabolism journal January 2019
Variation in expression of the HECT E3 ligase UPL3 modulates LEC2 levels, gene expression, seed size and crop yields in Brassica napus posted_content August 2018
Engineering storage capacity for volatile sesquiterpenes in Nicotiana benthamiana leaves journal May 2018
Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication journal July 2019
Overexpression of a Transcription Factor Increases Lipid Content in a Woody Perennial Jatropha curcas journal October 2018
The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network journal August 2018
Glycation of Plant Proteins: Regulatory Roles and Interplay with Sugar Signalling? journal May 2019
WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis journal July 2019
Oil body biogenesis and biotechnology in legume seeds journal September 2017
Molecular Basis of Plant Oil Biosynthesis: Insights Gained From Studying the WRINKLED1 Transcription Factor journal February 2020
Atypical Splicing Accompanied by Skipping Conserved Micro-exons Produces Unique WRINKLED1, An AP2 Domain Transcription Factor in Rice Plants journal July 2019

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