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

Journal Article · · Frontiers in Plant Science

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.

Research Organization:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0012704; KC0304000
OSTI ID:
1879918
Alternate ID(s):
OSTI ID: 1878302
Report Number(s):
BNL-223169-2022-JAAM; 955589
Journal Information:
Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 13; ISSN 1664-462X
Publisher:
Frontiers Media SACopyright Statement
Country of Publication:
Switzerland
Language:
English

References (126)

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana journal March 2016
Large-Scale cis-Element Detection by Analysis of Correlated Expression and Sequence Conservation between Arabidopsis and Brassica oleracea   journal October 2006
PII is induced by WRINKLED1 and fine-tunes fatty acid composition in seeds of Arabidopsis thaliana: PII fine-tunes fatty acid composition in seeds journal September 2010
FIMO: scanning for occurrences of a given motif journal February 2011
The Mediator Complex MED15 Subunit Mediates Activation of Downstream Lipid-Related Genes by the WRINKLED1 Transcription Factor journal May 2016
Potato tuber expression of Arabidopsis WRINKLED1 increase triacylglycerol and membrane lipids while affecting central carbohydrate metabolism journal March 2016
A spatiotemporal analysis of enzymatic activities associated with carbon metabolism in wild-type and mutant embryos of Arabidopsis using in situ histochemistry journal April 2006
Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis: WRI1, enhancer of glycolytic and lipogenic genes journal December 2009
Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome journal August 2014
A New Set of Arabidopsis Expressed Sequence Tags from Developing Seeds. The Metabolic Pathway from Carbohydrates to Seed Oil, journal December 2000
Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling journal June 2002
BnWRI1 coordinates fatty acid biosynthesis and photosynthesis pathways during oil accumulation in rapeseed journal March 2014
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation journal May 2010
Metabolic cartography: experimental quantification of metabolic fluxes from isotopic labelling studies journal February 2012
Database resources of the National Center for Biotechnology Information journal November 2017
Molecular and biochemical characterizations of a plastidic glycerol-3-phosphate dehydrogenase from Arabidopsis journal October 2001
Positional distribution of transcription factor binding sites in Arabidopsis thaliana journal April 2016
Potential targets of VIVIPAROUS1/ABI3-LIKE1 (VAL1) repression in developing Arabidopsis thaliana embryos journal January 2016
Improving the Annotation of Arabidopsis lyrata Using RNA-Seq Data journal September 2015
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Lipid exchanges drove the evolution of mutualism during plant terrestrialization journal May 2021
Syntenic gene analysis between Brassica rapa and other Brassicaceae species journal January 2012
Computational Approaches to Identify Promoters and cis-Regulatory Elements in Plant Genomes journal July 2003
WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis journal September 2004
DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA journal November 2000
Characterization and expression analysis of genes encoding ? and ? carbonic anhydrases in Arabidopsis journal May 2007
The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community journal January 2003
De novo assembly of the pennycress ( Thlaspi arvense ) transcriptome provides tools for the development of a winter cover crop and biodiesel feedstock journal August 2013
WRINKLED1 transcription factor: How much do we know about its regulatory mechanism? journal July 2018
Molecular and epigenetic regulations and functions of the LAFL transcriptional regulators that control seed development journal May 2018
Acyl-Lipid Metabolism journal January 2013
Transitions in wheat endosperm metabolism upon transcriptional induction of oil accumulation by oat endosperm WRINKLED1 journal May 2020
N ONPHOTOSYNTHETIC M ETABOLISM IN P LASTIDS journal June 2000
Integration of a constraint-based metabolic model of Brassica napus developing seeds with 13C-metabolic flux analysis journal December 2014
Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds journal December 2004
Phylogenetic Analyses and GAGA-Motif Binding Studies of BBR/BPC Proteins Lend to Clues in GAGA-Motif Recognition and a Regulatory Role in Brassinosteroid Signaling journal April 2019
Inhibition of Arabidopsis chloroplast β-amylase BAM3 by maltotriose suggests a mechanism for the control of transitory leaf starch mobilisation journal February 2017
DAVID-WS: a stateful web service to facilitate gene/protein list analysis journal April 2012
Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis: Roles of BASIC PENTACYSTEINE genes journal April 2011
The genome of the extremophile crucifer Thellungiella parvula journal August 2011
The Capacity of Green Oilseeds to Utilize Photosynthesis to Drive Biosynthetic Processes journal September 2004
MEME SUITE: tools for motif discovery and searching journal May 2009
DNA binding sites: representation and discovery journal January 2000
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
Genome of Plant Maca ( Lepidium meyenii ) Illuminates Genomic Basis for High-Altitude Adaptation in the Central Andes journal July 2016
Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules journal September 2008
AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus journal September 2018
WRINKLED Transcription Factors Orchestrate Tissue-Specific Regulation of Fatty Acid Biosynthesis in Arabidopsis journal December 2012
An introduction to ROC analysis journal June 2006
ATTED-II v11: A Plant Gene Coexpression Database Using a Sample Balancing Technique by Subagging of Principal Components journal March 2022
Gene coexpression network analysis of oil biosynthesis in an interspecific backcross of oil palm journal July 2016
The Sequence Manipulation Suite: JavaScript Programs for Analyzing and Formatting Protein and DNA Sequences journal June 2000
Plastidial Phosphoglucose Isomerase Is an Important Determinant of Seed Yield through Its Involvement in Gibberellin-Mediated Reproductive Development and Storage Reserve Biosynthesis in Arabidopsis journal August 2018
ACTIVATOR of Spomin::LUC1/WRINKLED1 of Arabidopsis thaliana Transactivates Sugar-inducible Promoters journal April 2005
GenomicusPlants: A Web Resource to Study Genome Evolution in Flowering Plants journal November 2014
A Heteromeric Plastidic Pyruvate Kinase Complex Involved in Seed Oil Biosynthesis in Arabidopsis journal June 2007
Duplicate Maize Wrinkled1 Transcription Factors Activate Target Genes Involved in Seed Oil Biosynthesis journal April 2011
ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis journal January 2007
Applied bioinformatics for the identification of regulatory elements journal April 2004
The Reference Genome of the Halophytic Plant Eutrema salsugineum journal January 2013
bZIP67 Regulates the Omega-3 Fatty Acid Content of Arabidopsis Seed Oil by Activating FATTY ACID DESATURASE3 journal August 2013
An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions journal June 2013
Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues journal April 2016
NCBI BLAST: a better web interface journal May 2008
A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize journal September 2009
Seed Architecture Shapes Embryo Metabolism in Oilseed Rape journal May 2013
A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in Arabidopsis thaliana journal June 2014
Transcriptional transitions in Nicotiana benthamiana leaves upon induction of oil synthesis by WRINKLED1 homologs from diverse species and tissues journal August 2015
Medicago AP2-Domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal Symbiosis journal November 2018
Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning journal June 2011
wrinkled1 : A Novel, Low-Seed-Oil Mutant of Arabidopsis with a Deficiency in the Seed-Specific Regulation of Carbohydrate Metabolism journal September 1998
Mitochondrial Metabolism in Developing Embryos of Brassica napus journal September 2006
Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors journal June 2009
An annotated database of Arabidopsis mutants of acyl lipid metabolism journal December 2014
An Integrated Bioinformatics Analysis Reveals Divergent Evolutionary Pattern of Oil Biosynthesis in High- and Low-Oil Plants journal May 2016
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape journal May 2016
Biochemical and Molecular Inhibition of Plastidial Carbonic Anhydrase Reduces the Incorporation of Acetate into Lipids in Cotton Embryos and Tobacco Cell Suspensions and Leaves journal March 2002
The Sunflower WRINKLED1 Transcription Factor Regulates Fatty Acid Biosynthesis Genes through an AW Box Binding Sequence with a Particular Base Bias journal April 2022
Comparative deep transcriptional profiling of four developing oilseeds: Transcriptional profiling of oilseeds journal October 2011
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
Expression of the genes coding for plastidic acetyl-CoA carboxylase subunits is regulated by a location-sensitive transcription factor binding site journal June 2013
Genome-Wide Mapping of Histone H3 Lysine 4 Trimethylation (H3K4me3) and Its Involvement in Fatty Acid Biosynthesis in Sunflower Developing Seeds journal April 2021
Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis journal June 2009
Wrinkled1 Accelerates Flowering and Regulates Lipid Homeostasis between Oil Accumulation and Membrane Lipid Anabolism in Brassica napus journal November 2015
Transcriptional regulation of fatty acid production in higher plants: Molecular bases and biotechnological outcomes: The WRINKLED transcription factors journal August 2014
Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions journal March 2013
WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds journal March 2016
Identification, Purification, and Molecular Cloning of a Putative Plastidic Glucose Translocator journal May 2000
WRINKLED1 Regulates BIOTIN ATTACHMENT DOMAIN-CONTAINING Proteins that Inhibit Fatty Acid Synthesis journal June 2019
Compartmentation of Triacylglycerol Accumulation in Plants journal November 2011
Ectopic expression of WRI1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues journal September 2015
Non-conventional pathways enable pennycress (Thlaspi arvense L.) embryos to achieve high efficiency of oil biosynthesis journal February 2020
Approaches for Extracting Practical Information from Gene Co-expression Networks in Plant Biology journal January 2007
Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana journal December 2010
Quantitative Multilevel Analysis of Central Metabolism in Developing Oilseeds of Oilseed Rape during in Vitro Culture journal May 2015
Transcription-driven chromatin repression of Intragenic transcription start sites journal February 2019
Arabidopsis Fructokinases Are Important for Seed Oil Accumulation and Vascular Development journal January 2017
Starch turnover in developing oilseed embryos journal June 2010
FaBox: an online toolbox for fasta sequences journal November 2007
Involvement of a Glycerol-3-Phosphate Dehydrogenase in Modulating the NADH/NAD+ Ratio Provides Evidence of a Mitochondrial Glycerol-3-Phosphate Shuttle in Arabidopsis journal January 2006
A Flux Model of Glycolysis and the Oxidative Pentosephosphate Pathway in Developing Brassica napus Embryos journal May 2003
The Capsella rubella genome and the genomic consequences of rapid mating system evolution journal June 2013
WRINKLED1, A Ubiquitous Regulator in Oil Accumulating Tissues from Arabidopsis Embryos to Oil Palm Mesocarp journal July 2013
WebLogo: A Sequence Logo Generator journal May 2004
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources journal December 2008
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools journal December 2011
WRINKLED1 transcription factor orchestrates the regulation of carbon partitioning for C18:1 (oleic acid) accumulation in Siberian apricot kernel journal February 2019
A polymorphic (GA/CT)n- SSR influences promoter activity of Tryptophan decarboxylase gene in Catharanthus roseus L. Don journal September 2016
Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed journal July 2005
Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean ( Glycine max ) journal June 2019
AtDGAT2 is a functional acyl-CoA:diacylglycerol acyltransferase and displays different acyl-CoA substrate preferences than AtDGAT1 journal June 2013
The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure journal April 2014
Analysis of Metabolic Flux Phenotypes for Two Arabidopsis Mutants with Severe Impairment in Seed Storage Lipid Synthesis journal September 2009
Cuticular wax biosynthesis is positively regulated by WRINKLED4, an AP2/ERF-type transcription factor, in Arabidopsis stems journal August 2016
Differential Activation of Partially Redundant Δ9 Stearoyl-ACP Desaturase Genes Is Critical for Omega-9 Monounsaturated Fatty Acid Biosynthesis During Seed Development in Arabidopsis journal September 2020
Carbon flux and fatty acid synthesis in plants journal March 2002
Sunflower (Helianthus annuus) fatty acid synthase complex: β-Ketoacyl-[acyl carrier protein] reductase genes journal September 2021
The embryonic transcriptome of Arabidopsis thaliana journal January 2019
WRINKLED1 homologs highly and functionally express in oil-rich endosperms of oat and castor journal October 2019
Absence of a simple code: how transcription factors read the genome journal September 2014
Cabbage family affairs: the evolutionary history of Brassicaceae journal February 2011
The Cardamine hirsuta genome offers insight into the evolution of morphological diversity journal October 2016
WRINKLED1, a “Master Regulator” in Transcriptional Control of Plant Oil Biosynthesis journal July 2019
An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis journal October 2009
The Arabidopsis WRINKLED1 transcription factor affects auxin homeostasis in roots journal July 2017
Identification and biochemical characterization of the fructokinase gene family in Arabidopsis thaliana journal April 2017