Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis

Several lipid-transfer proteins were reported to modulate the plant response to biotic stress; however, whether lipid-transfer proteins are also involved in abiotic stress remains unknown. This study characterized the function of a lipid-transfer protein, LTP3, during freezing and drought stress. LTP3 was expressed ubiquitously and the LTP3 protein was localized to the cytoplasm. A biochemical study showed that LTP3 was able to bind to lipids. Overexpression of LTP3 resulted in constitutively enhanced freezing tolerance without affecting the expression of CBFs and their target COR genes. Further analyses showed that LTP3 was positively regulated by MYB96 via the direct binding to the LTP3 promoter; consistently, transgenic plants overexpressing MYB96 exhibited enhanced freezing tolerance. This study also found that the loss-of-function mutant ltp3 was sensitive to drought stress, whereas overexpressing plants were drought tolerant, phenotypes reminiscent of myb96 mutant plants and MYB96-overexpressing plants. Taken together, these results demonstrate that LTP3 acts as a target of MYB96 to be involved in plant tolerance to freezing and drought stress.

• Publication year

  2013

• Venue

  Journal of Experimental Botany

• Publication date

  2013-02-11

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/jxb/ert040PMID 23404903PMCID 3617838
• 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.

• A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis[W][OA]

  2012cited by this paper
• Ethylene Signaling Negatively Regulates Freezing Tolerance by Repressing Expression of CBF and Type-A ARR Genes in Arabidopsis[W][OA]

  2012influential reference
• The MYB96 Transcription Factor Regulates Cuticular Wax Biosynthesis under Drought Conditions in Arabidopsis[W]

  2011influential reference
• A Gain-of-Function Mutation in the Arabidopsis Disease Resistance Gene RPP4 Confers Sensitivity to Low Temperature1[W][OA]

  2010cited by this paper
• A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis.

  2010cited by this paper
• MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis.

  2010cited by this paper
• The MYB96 Transcription Factor Mediates Abscisic Acid Signaling during Drought Stress Response in Arabidopsis1[W]

  2009cited by this paper
• Identification of SFR6, a key component in cold acclimation acting post-translationally on CBF function.

  2009cited by this paper
• Priming in Systemic Plant Immunity

  2009cited by this paper
• Arabidopsis LTPG Is a Glycosylphosphatidylinositol-Anchored Lipid Transfer Protein Required for Export of Lipids to the Plant Surface[W][OA]

  2009cited by this paper
• Roles for Arabidopsis CAMTA Transcription Factors in Cold-Regulated Gene Expression and Freezing Tolerance[W][OA]

  2009cited by this paper
• ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION DEFICIENT2 Expression to Negatively Regulate Plant Innate Immunity in Arabidopsis[W][OA]

  2009cited by this paper
• A Gain-of-Function Mutation of Arabidopsis Lipid Transfer Protein 5 Disturbs Pollen Tube Tip Growth and Fertilization[C][W]

  2009cited by this paper
• The biochemistry and biology of extracellular plant lipid‐transfer proteins (LTPs)

  2008cited by this paper
• Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance

  2008cited by this paper
• SIZ1-Mediated Sumoylation of ICE1 Controls CBF3/DREB1A Expression and Freezing Tolerance in Arabidopsis[W][OA]

  2007cited by this paper
• Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis

  2007cited by this paper
• Overexpression of AtMYB44 Enhances Stomatal Closure to Confer Abiotic Stress Tolerance in Transgenic Arabidopsis1[C][W][OA]

  2007cited by this paper
• STABILIZED1, a Stress-Upregulated Nuclear Protein, Is Required for Pre-mRNA Splicing, mRNA Turnover, and Stress Tolerance in Arabidopsis[W]

  2006cited by this paper
• A Putative Arabidopsis Nucleoporin, AtNUP160, Is Critical for RNA Export and Required for Plant Tolerance to Cold Stress

  2006cited by this paper
• A R2R3 Type MYB Transcription Factor Is Involved in the Cold Regulation of CBF Genes and in Acquired Freezing Tolerance*

  2006influential reference
• The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1.

  2006cited by this paper
• Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.

  2006cited by this paper
• A DEAD Box RNA Helicase Is Essential for mRNA Export and Important for Development and Stress Responses in Arabidopsis

  2005cited by this paper
• A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance.

  2005cited by this paper
• Profiling histone modification patterns in plants using genomic tiling microarrays

  2005cited by this paper
• Lipid Transfer Proteins Enhance Cell Wall Extension in Tobaccow⃞

  2005cited by this paper
• Arabidopsis Transcriptional Activators CBF1, CBF2, and CBF3 have Matching Functional Activities

  2004cited by this paper
• Modulation of the biological activity of a tobacco LTP1 by lipid complexation.

  2004cited by this paper
• Fatty acid interactions with proteins: what X-ray crystal and NMR solution structures tell us.

  2004cited by this paper
• ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis.

  2003cited by this paper
• LOS2, a genetic locus required for cold‐responsive gene transcription encodes a bi‐functional enolase

  2002cited by this paper
• Profiling Membrane Lipids in Plant Stress Responses

  2002cited by this paper
• A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis

  2002cited by this paper
• Cold comfort farm: the acclimation of plants to freezing temperatures.

  2000cited by this paper
• Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants.

  2000influential reference
• STEROL METHYLTRANSFERASE 1 Controls the Level of Cholesterol in Plants

  2000cited by this paper
• Lipid-transfer proteins from plants: Structure and binding properties

  1999cited by this paper
• Cold-induced freezing tolerance in Arabidopsis.

  1999cited by this paper
• Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.

  1999cited by this paper
• Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana.

  1999cited by this paper
• PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms.

  1999cited by this paper
• Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis

  1998cited by this paper
• Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant.

  1998cited by this paper
• Characterisation of acyl binding by a plant lipid-transfer protein.

  1998cited by this paper
• Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance.

  1998cited by this paper
• Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.

  1998cited by this paper
• Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana.

  1998cited by this paper
• Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2.

  1997cited by this paper
• Membrane Fluidity and Temperature Perception

  1997cited by this paper
• Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance.

  1996cited by this paper
• LIPID-TRANSFER PROTEINS IN PLANTS.

  1996cited by this paper
• CHILLING SENSITIVITY IN PLANTS AND CYANOBACTERIA: The Crucial Contribution of Membrane Lipids.

  1996cited by this paper
• An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence.

  1993cited by this paper
• Cell-specific expression of the carrot EP2 lipid transfer protein gene.

  1991cited by this paper
• Purification and characterization of a spinach-leaf protein capable of transferring phospholipids from liposomes to mitochondria or chloroplasts.

  1984cited by this paper
• Rapid determination of free proline for water-stress studies

  1973cited by this paper
• The mode of action of the bipyridylium herbicides, paraquat and diquat.

  1971cited by this paper

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  2026cites this paper
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  2026cites this paper
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  2026cites this paper
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  2025cites this paper
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  2025cites this paper
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  2021influential citation
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