The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation

Highlight This study reveals that the transcription factor PHR1 controls phospholipid/glycolipid substitution during P starvation, and that Arabidopsis accumulates triacylglycerol during P starvation. In roots this phenotype is also under control of PHR1.

• Publication year

  2015

• Venue

  Journal of Experimental Botany

• Publication date

  2015-02-13

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/jxb/eru535PMID 25680792PMCID 4378627
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• gplots: Various R Programming Tools for Plotting Data

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• Phosphate starvation and membrane lipid remodeling in seed plants.

  2013cited by this paper
• Triacylglycerol accumulation and change in fatty acid content of four marine oleaginous microalgae under nutrient limitation and at different culture ages

  2013cited by this paper
• WRINKLED Transcription Factors Orchestrate Tissue-Specific Regulation of Fatty Acid Biosynthesis in Arabidopsis[W]

  2012cited by this paper
• Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana.

  2012cited by this paper
• Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems.

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• The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation

  2012cited by this paper
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• Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light.

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• Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation.

  2011cited by this paper
• Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis.

  2010influential reference
• A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis

  2010influential reference
• Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation.

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  2009influential reference
• DGAT1 and PDAT1 Acyltransferases Have Overlapping Functions in Arabidopsis Triacylglycerol Biosynthesis and Are Essential for Normal Pollen and Seed Development[W][OA]

  2009cited by this paper
• Identification of Nutrient-Responsive Arabidopsis and Rapeseed MicroRNAs by Comprehensive Real-Time Polymerase Chain Reaction Profiling and Small RNA Sequencing1[C][W][OA]

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• Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis.

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• Root tip contact with low-phosphate media reprograms plant root architecture

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  2007cited by this paper
• Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus.

  2007influential reference
• WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis1[C][W][OA]

  2007cited by this paper
• PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants1[W][OA]

  2006influential reference
• Faculty Opinions recommendation of Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis.

  2006cited by this paper
• Genome-Wide Analysis of the Arabidopsis Leaf Transcriptome Reveals Interaction of Phosphate and Sugar Metabolism1[W]

  2006cited by this paper
• Quantitative Profiling of Arabidopsis Polar Glycerolipids in Response to Phosphorus Starvation. Roles of Phospholipases Dζ1 and Dζ2 in Phosphatidylcholine Hydrolysis and Digalactosyldiacylglycerol Accumulation in Phosphorus-Starved Plants1[W]

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• WRI1 Is Required for Seed Germination and Seedling Establishment1

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• pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene1[W]

  2006cited by this paper
• Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots.

  2006cited by this paper
• Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis1[w]

  2005cited by this paper
• A miRNA involved in phosphate-starvation response in Arabidopsis.

  2005cited by this paper
• A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation.

  2005influential reference
• A Novel Phosphatidylcholine-hydrolyzing Phospholipase C Induced by Phosphate Starvation in Arabidopsis*

  2005influential reference
• The transcriptional control of plant responses to phosphate limitation.

  2004cited by this paper
• Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence

  2004influential reference
• Phosphate Acquisition

  2004cited by this paper
• Disruption of the Two Digalactosyldiacylglycerol Synthase Genes DGD1 and DGD2 in Arabidopsis Reveals the Existence of an Additional Enzyme of Galactolipid Synthesis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016675.

  2003cited by this paper
• A Role for Diacylglycerol Acyltransferase during Leaf Senescence1

  2002cited by this paper
• A rabidopsis thaliana

  2002cited by this paper
• Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply.

  2002cited by this paper
• DGD2, an Arabidopsis Gene Encoding a UDP-Galactose-dependent Digalactosyldiacylglycerol Synthase Is Expressed during Growth under Phosphate-limiting Conditions*

  2002cited by this paper
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  2002cited by this paper
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  2002cited by this paper
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  2001cited by this paper
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  2001cited by this paper
• A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.

  2001influential reference
• DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis.

  2000cited by this paper
• EFFECT OF NUTRIENT AVAILABILITY ON THE BIOCHEMICAL AND ELEMENTAL STOICHIOMETRY IN THE FRESHWATER DIATOM STEPHANODISCUS MINUTULUS (BACILLARIOPHYCEAE)*

  2000cited by this paper
• Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1.

  1999cited by this paper
• Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana.

  1998influential reference
• Growth and reproduction of Daphnia galeata in response to changes in fatty acids, phosphorus, and nitrogen in Chlamydomonas reinhardtii

  1997cited by this paper
• The responses of wild‐type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation

  1997cited by this paper
• Gentleman R: R: A language for data analysis and graphics

  1996cited by this paper
• Regulation of the Amount of Starch in Plant Tissues by ADP Glucose Pyrophosphorylase

  1992cited by this paper
• Mutant of Arabidopsis deficient in xylem loading of phosphate.

  1991cited by this paper
• Efficient lipid staining in plant material with sudan red 7B or fluorol [correction of fluoral] yellow 088 in polyethylene glycol-glycerol.

  1991cited by this paper
• Glycerolipid Synthesis: Biochemistry and Regulation

  1991cited by this paper
• The effect of phosphate deprivation on protein synthesis and fixed carbon storage reserves in Brassica nigra suspension cells

  1990cited by this paper
• Influence of Phosphorus Nutrition on Growth and Carbon Partitioning in Glycine max.

  1989cited by this paper
• Position and pairing of fatty acids in phosphatidylglycerol from pea leaf chloroplasts and mitochondria

  1989cited by this paper
• Plasma Membrane Lipid Alterations Associated with Cold Acclimation of Winter Rye Seedlings (Secale cereale L. cv Puma).

  1987cited by this paper
• Phosphatidylglycerol and chilling sensitivity in plants.

  1985cited by this paper
• Starch, sucrose biosynthesis and partition of carbon in plants are regulated by orthophosphate and triose-phosphates

  1984cited by this paper
• The effect of nitrogen and phosphorus on starch accumulation and net photosynthesis in two variants of Panicum maximum Jacq.

  1983cited by this paper

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