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Title: An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development

Abstract

The transcription factor WRINKLED1 ( WRI1 ) is known as a master regulator of fatty acid synthesis in developing oilseeds of Arabidopsis thaliana and other species. WRI1 is known to directly stimulate the expression of many fatty acid biosynthetic enzymes and a few targets in the lower part of the glycolytic pathway. However, it remains unclear to what extent and how the conversion of sugars into fatty acid biosynthetic precursors is controlled by WRI 1. To shortlist possible gene targets for future in-planta experimental validation, here we present a strategy that combines phylogenetic foot printing of cis-regulatory elements with additional layers of evidence. Upstream regions of protein-encoding genes in A. thaliana were searched for the previously described DNA-binding consensus for WRI1, the ASML1/WRI1 (AW)-box. For about 900 genes, AW-box sites were found to be conserved across orthologous upstream regions in 11 related species of the crucifer family. For 145 select potential target genes identified this way, affinity of upstream AW-box sequences to WRI1 was assayed by Microscale Thermophoresis. This allowed definition of a refined WRI1 DNA-binding consensus. We find that known WRI1 gene targets are predictable with good confidence when upstream AW-sites are phylogenetically conserved, specifically binding WRI1 in themore » in vitro assay, positioned in proximity to the transcriptional start site, and if the gene is co-expressed with WRI1 during seed development. When targets predicted in this way are mapped to central metabolism, a conserved regulatory blueprint emerges that infers concerted control of contiguous pathway sections in glycolysis and fatty acid biosynthesis by WRI1. Several of the newly predicted targets are in the upper glycolysis pathway and the pentose phosphate pathway. Of these, plastidic isoforms of fructokinase ( FRK 3) and of phosphoglucose isomerase ( PGI 1) are particularly corroborated by previously reported seed phenotypes of respective null mutations.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1879918
Alternate Identifier(s):
OSTI ID: 1878302
Report Number(s):
BNL-223169-2022-JAAM
Journal ID: ISSN 1664-462X; 955589
Grant/Contract Number:  
SC0012704; KC0304000
Resource Type:
Journal Article: Published Article
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Name: Frontiers in Plant Science Journal Volume: 13; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; aArabidopsis; brassicaceae; triacyl glycerol; cis-regulatory; element; transcription; factor; binding; motif; seed; development; central metabolism; fatty acid; biosynthesis

Citation Formats

Kuczynski, Cathleen, McCorkle, Sean, Keereetaweep, Jantana, Shanklin, John, and Schwender, Jorg. An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development. Switzerland: N. p., 2022. Web. doi:10.3389/fpls.2022.955589.
Kuczynski, Cathleen, McCorkle, Sean, Keereetaweep, Jantana, Shanklin, John, & Schwender, Jorg. An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development. Switzerland. https://doi.org/10.3389/fpls.2022.955589
Kuczynski, Cathleen, McCorkle, Sean, Keereetaweep, Jantana, Shanklin, John, and Schwender, Jorg. 2022. "An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development". Switzerland. https://doi.org/10.3389/fpls.2022.955589.
@article{osti_1879918,
title = {An expanded role for the transcription factor WRINKLED1 in the biosynthesis of triacylglycerols during seed development},
author = {Kuczynski, Cathleen and McCorkle, Sean and Keereetaweep, Jantana and Shanklin, John and Schwender, Jorg},
abstractNote = {The transcription factor WRINKLED1 ( WRI1 ) is known as a master regulator of fatty acid synthesis in developing oilseeds of Arabidopsis thaliana and other species. WRI1 is known to directly stimulate the expression of many fatty acid biosynthetic enzymes and a few targets in the lower part of the glycolytic pathway. However, it remains unclear to what extent and how the conversion of sugars into fatty acid biosynthetic precursors is controlled by WRI 1. To shortlist possible gene targets for future in-planta experimental validation, here we present a strategy that combines phylogenetic foot printing of cis-regulatory elements with additional layers of evidence. Upstream regions of protein-encoding genes in A. thaliana were searched for the previously described DNA-binding consensus for WRI1, the ASML1/WRI1 (AW)-box. For about 900 genes, AW-box sites were found to be conserved across orthologous upstream regions in 11 related species of the crucifer family. For 145 select potential target genes identified this way, affinity of upstream AW-box sequences to WRI1 was assayed by Microscale Thermophoresis. This allowed definition of a refined WRI1 DNA-binding consensus. We find that known WRI1 gene targets are predictable with good confidence when upstream AW-sites are phylogenetically conserved, specifically binding WRI1 in the in vitro assay, positioned in proximity to the transcriptional start site, and if the gene is co-expressed with WRI1 during seed development. When targets predicted in this way are mapped to central metabolism, a conserved regulatory blueprint emerges that infers concerted control of contiguous pathway sections in glycolysis and fatty acid biosynthesis by WRI1. Several of the newly predicted targets are in the upper glycolysis pathway and the pentose phosphate pathway. Of these, plastidic isoforms of fructokinase ( FRK 3) and of phosphoglucose isomerase ( PGI 1) are particularly corroborated by previously reported seed phenotypes of respective null mutations.},
doi = {10.3389/fpls.2022.955589},
url = {https://www.osti.gov/biblio/1879918}, journal = {Frontiers in Plant Science},
issn = {1664-462X},
number = ,
volume = 13,
place = {Switzerland},
year = {Fri Aug 05 00:00:00 EDT 2022},
month = {Fri Aug 05 00:00:00 EDT 2022}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.3389/fpls.2022.955589

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