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Title: Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling

Abstract

Global climate changes inversely affect our ability to grow the food required for an increasing world population. To combat future crop loss due to abiotic stress, we need to understand the signals responsible for changes in plant development and the resulting adaptations, especially the signaling molecules traveling long-distance through the plant phloem. Using a proteomics approach, we had identified several putative lipid-binding proteins in the phloem exudates. Simultaneously, we identified several complex lipids as well as jasmonates. These findings prompted us to propose that phloem (phospho-) lipids could act as long-distance developmental signals in response to abiotic stress, and that they are released, sensed, and moved by phloem lipid-binding proteins (Benning et al., 2012). Indeed, the proteins we identified include lipases that could release a signaling lipid into the phloem, putative receptor components, and proteins that could mediate lipid-movement. To test this possible protein-based lipid-signaling pathway, three of the proteins, which could potentially act in a relay, are characterized here: (I) a putative GDSL-motif lipase (II) a PIG-P-like protein, with a possible receptor-like function; (III) and PLAFP (phloem lipid-associated family protein), a predicted lipid-binding protein of unknown function. Here we show that all three proteins bind lipids, in particular phosphatidicmore » acid (PtdOH), which is known to participate in intracellular stress signaling. Genes encoding these proteins are expressed in the vasculature, a prerequisite for phloem transport. Cellular localization studies show that the proteins are not retained in the endoplasmic reticulum but surround the cell in a spotted pattern that has been previously observed with receptors and plasmodesmatal proteins. Abiotic signals that induce the production of PtdOH also regulate the expression of GDSL-lipase and PLAFP, albeit in opposite patterns. Our findings suggest that while all three proteins are indeed lipid-binding and act in the vasculature possibly in a function related to long-distance signaling, the three proteins do not act in the same but rather in distinct pathways. Furthermore, it points toward PLAFP as a prime candidate to investigate long-distance lipid signaling in the plant drought response.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1257760
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; abiotic stress; lipid signaling; lipid-binding proteins; phloem; phospholipids

Citation Formats

Barbaglia, Allison M., Tamot, Banita, Greve, Veronica, and Hoffmann-Benning, Susanne. Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.00563.
Barbaglia, Allison M., Tamot, Banita, Greve, Veronica, & Hoffmann-Benning, Susanne. Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling. United States. https://doi.org/10.3389/fpls.2016.00563
Barbaglia, Allison M., Tamot, Banita, Greve, Veronica, and Hoffmann-Benning, Susanne. 2016. "Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling". United States. https://doi.org/10.3389/fpls.2016.00563. https://www.osti.gov/servlets/purl/1257760.
@article{osti_1257760,
title = {Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling},
author = {Barbaglia, Allison M. and Tamot, Banita and Greve, Veronica and Hoffmann-Benning, Susanne},
abstractNote = {Global climate changes inversely affect our ability to grow the food required for an increasing world population. To combat future crop loss due to abiotic stress, we need to understand the signals responsible for changes in plant development and the resulting adaptations, especially the signaling molecules traveling long-distance through the plant phloem. Using a proteomics approach, we had identified several putative lipid-binding proteins in the phloem exudates. Simultaneously, we identified several complex lipids as well as jasmonates. These findings prompted us to propose that phloem (phospho-) lipids could act as long-distance developmental signals in response to abiotic stress, and that they are released, sensed, and moved by phloem lipid-binding proteins (Benning et al., 2012). Indeed, the proteins we identified include lipases that could release a signaling lipid into the phloem, putative receptor components, and proteins that could mediate lipid-movement. To test this possible protein-based lipid-signaling pathway, three of the proteins, which could potentially act in a relay, are characterized here: (I) a putative GDSL-motif lipase (II) a PIG-P-like protein, with a possible receptor-like function; (III) and PLAFP (phloem lipid-associated family protein), a predicted lipid-binding protein of unknown function. Here we show that all three proteins bind lipids, in particular phosphatidic acid (PtdOH), which is known to participate in intracellular stress signaling. Genes encoding these proteins are expressed in the vasculature, a prerequisite for phloem transport. Cellular localization studies show that the proteins are not retained in the endoplasmic reticulum but surround the cell in a spotted pattern that has been previously observed with receptors and plasmodesmatal proteins. Abiotic signals that induce the production of PtdOH also regulate the expression of GDSL-lipase and PLAFP, albeit in opposite patterns. Our findings suggest that while all three proteins are indeed lipid-binding and act in the vasculature possibly in a function related to long-distance signaling, the three proteins do not act in the same but rather in distinct pathways. Furthermore, it points toward PLAFP as a prime candidate to investigate long-distance lipid signaling in the plant drought response.},
doi = {10.3389/fpls.2016.00563},
url = {https://www.osti.gov/biblio/1257760}, journal = {Frontiers in Plant Science},
issn = {1664-462X},
number = ,
volume = 7,
place = {United States},
year = {Thu Apr 28 00:00:00 EDT 2016},
month = {Thu Apr 28 00:00:00 EDT 2016}
}

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Cited by: 18 works
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Works referenced in this record:

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journal, March 2012


Analysis of the Poplar Phloem Proteome and Its Response to Leaf Wounding
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Plant phloem sterol content: forms, putative functions, and implications for phloem-feeding insects
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The tomato phosphatidylinositol-phospholipase C2 (SlPLC2) is required for defense gene induction by the fungal elicitor xylanase
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Phloem RNA-binding proteins as potential components of the long-distance RNA transport system
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Phloem-mobile messenger RNAs and root development
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Cooperative Function of PLDδ and PLDα1 in Abscisic Acid-Induced Stomatal Closure in Arabidopsis
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Proteome study of the phloem sap of pumpkin using multidimensional protein identification technology
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Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants
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New Aspects of Phloem-Mediated Long-Distance Lipid Signaling in Plants
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The Arabidopsis PLAT Domain Protein1 Is Critically Involved in Abiotic Stress Tolerance
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Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis
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Overexpression of the Arabidopsis 10-Kilodalton Acyl-Coenzyme A-Binding Protein ACBP6 Enhances Freezing Tolerance
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Priming in Systemic Plant Immunity
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Plant phospholipid signaling: “in a nutshell”
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Proteomics of curcurbit phloem exudate reveals a network of defence proteins
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Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering
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Structural Basis of Wnt Recognition by Frizzled
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Molecular, cellular, and physiological responses to phosphatidic acid formation in plants
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Hormonal regulation of tomato gibberellin 20-oxidase1 expressed in Arabidopsis
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Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis
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The broccoli (Brassica oleracea) phloem tissue proteome
journal, January 2013


Proteomic characterization of copper stress response inCannabis sativa roots
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Castor (Ricinus communis L.) Rc-LOX5 plays important role in wilt resistance
journal, February 2013


Phloem Ultrastructure and Pressure Flow: Sieve-Element-Occlusion-Related Agglomerations Do Not Affect Translocation
journal, December 2011


Phosphatidylinositol 4,5-Bisphosphate Influences PIN Polarization by Controlling Clathrin-Mediated Membrane Trafficking in Arabidopsis
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Nano Scale Proteomics Revealed the Presence of Regulatory Proteins Including Three FT-Like proteins in Phloem and Xylem Saps from Rice
journal, May 2008


S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
journal, June 2002


The Arabidopsis PLAT Domain Protein1 Is Critically Involved in Abiotic Stress Tolerance
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Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought
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Phosphatidic Acid Binds to Cytosolic Glyceraldehyde-3-phosphate Dehydrogenase and Promotes Its Cleavage in Arabidopsis
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Spontaneous Curvature of Phosphatidic Acid and Lysophosphatidic Acid
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Long-Distance Phloem Transport of Glucosinolates in Arabidopsis
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Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana
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Lipid signaling
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Phosphoinositide-signaling is one component of a robust plant defense response
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Plant sterols and host plant suitability for a phloem-feeding insect: Phloem sterols available to aphids
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Transportation of de novo synthesized jasmonoyl isoleucine in tomato
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The PLAT domain: a new piece in the PKD1 puzzle
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Protein profile of Lupinus texensis phloem sap exudates: Searching for Fe- and Zn-containing proteins
journal, July 2013


Secretome Analysis Reveals an Arabidopsis Lipase Involved in Defense against Alternaria brassicicola
journal, August 2005


Proteomic characterization of copper stress response inCannabis sativa roots
journal, April 2007


The tomato phosphatidylinositol-phospholipase C2 (SlPLC2) is required for defense gene induction by the fungal elicitor xylanase
journal, July 2014


Turnover of Soluble Proteins in the Wheat Sieve Tube
journal, November 1992


Signaling by small metabolites in systemic acquired resistance
journal, May 2014


Functional Convergence of Oxylipin and Abscisic Acid Pathways Controls Stomatal Closure in Response to Drought
journal, January 2014


Symplasmic protein and RNA traffic: regulatory points and regulatory factors
journal, December 2003


Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse
journal, January 2000


An abietane diterpenoid is a potent activator of systemic acquired resistance: Plant defense against pathogen
journal, April 2012


Phloem-exudate proteome analysis of response to insect brown plant-hopper in rice
journal, July 2015


Characterisation of microRNAs from apple (Malus domestica 'Royal Gala') vascular tissue and phloem sap
journal, January 2010


Structural Basis of Wnt Recognition by Frizzled
journal, May 2012


Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates
journal, January 2007


Molecular, cellular, and physiological responses to phosphatidic acid formation in plants
journal, March 2011


Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis
journal, October 2009


Proteomics of curcurbit phloem exudate reveals a network of defence proteins
journal, June 2004


Phloem Transport: Cellular Pathways and Molecular Trafficking
journal, June 2009


Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling
journal, February 2009


Nano Scale Proteomics Revealed the Presence of Regulatory Proteins Including Three FT-Like proteins in Phloem and Xylem Saps from Rice
journal, May 2008


Phosphatidic acid, a versatile water-stress signal in roots
journal, January 2013


Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants
journal, March 2011


Signaling functions of phosphatidic acid
journal, May 2006


Analysis of the Pumpkin Phloem Proteome Provides Insights into Angiosperm Sieve Tube Function
journal, October 2008


Connections between Sphingosine Kinase and Phospholipase D in the Abscisic Acid Signaling Pathway in Arabidopsis
journal, January 2012


Towards the proteome ofBrassica napus phloem sap
journal, February 2006


Long-Distance Phloem Transport of Glucosinolates in Arabidopsis
journal, September 2001


Isolation and characterization of lipid in phloem sap of canola
journal, February 2002


Transportation of de novo synthesized jasmonoyl isoleucine in tomato
journal, November 2012


Plasmodesmata – bridging the gap between neighboring plant cells
journal, October 2009


Glycerol-3-phosphate and systemic immunity
journal, November 2011


The Role of Phosphoinositides and Inositol Phosphates in Plant Cell Signaling
book, January 2013


Lipid signaling
journal, June 2004


The Plant Vascular System: Evolution, Development and Functions F
journal, April 2013


Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis
journal, March 2002


Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants
journal, October 1999


Spontaneous Curvature of Phosphatidic Acid and Lysophosphatidic Acid
journal, February 2005


The Xylem and Phloem Transcriptomes from Secondary Tissues of the Arabidopsis Root-Hypocotyl
journal, May 2005


MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis
journal, March 2008


Phloem small RNAs, nutrient stress responses, and systemic mobility
journal, January 2010


Isolation and Expression Analysis of a GDSL-like Lipase Gene from Brassica napus L.
journal, May 2006


Plant sterols and host plant suitability for a phloem-feeding insect: Phloem sterols available to aphids
journal, November 2010


Collection and Analysis of Arabidopsis Phloem Exudates Using the EDTA-facilitated Method
journal, January 2013


Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.)
journal, January 2011


Phosphatidic acid, a versatile water-stress signal in roots
journal, January 2013


Annexins - unique membrane binding proteins with diverse functions
journal, June 2004


Turnover of Soluble Proteins in the Wheat Sieve Tube
journal, November 1992


Priming in Systemic Plant Immunity
journal, April 2009


Function and regulation of phospholipid signalling in plants
journal, June 2009


Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates
journal, January 2007


PPARs at the crossroads of lipid signaling and inflammation
journal, July 2012


A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking
journal, July 2006


Surface structure and properties of plant seed oil bodies
journal, April 1992


Cooperative Function of PLDδ and PLDα1 in Abscisic Acid-Induced Stomatal Closure in Arabidopsis
journal, March 2012


Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling
journal, February 2009


Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998


New Aspects of Phloem-Mediated Long-Distance Lipid Signaling in Plants
journal, January 2012


Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones
journal, May 1995


Phosphoinositide-signaling is one component of a robust plant defense response
journal, June 2014


Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity
journal, April 2010


Analysis of the Poplar Phloem Proteome and Its Response to Leaf Wounding
journal, May 2009


A Systemic Small RNA Signaling System in Plants
journal, July 2004


The structure of “defective in induced resistance” protein of Arabidopsis thaliana , DIR1, reveals a new type of lipid transfer protein
journal, September 2008


Phloem-mobile messenger RNAs and root development
journal, January 2013


Phloem RNA-binding proteins as potential components of the long-distance RNA transport system
journal, January 2013


Plant phloem sterol content: forms, putative functions, and implications for phloem-feeding insects
journal, January 2013


GDSL family of serine esterases/lipases
journal, November 2004


Lipid signaling in plants
journal, January 2013


Systemic transport of RNA in plants
journal, February 2000


Phloem Ultrastructure and Pressure Flow: Sieve-Element-Occlusion-Related Agglomerations Do Not Affect Translocation
journal, December 2011


Signaling functions of phosphatidic acid
journal, May 2006


Salicylic Acid in Plant Disease Resistance
book, January 2007


The Xylem and Phloem Transcriptomes from Secondary Tissues of the Arabidopsis Root-Hypocotyl
journal, May 2005


Oxylipin metabolism in response to stress
journal, June 2002


Phloem Transport: Cellular Pathways and Molecular Trafficking
journal, June 2009


The Plant Vascular System: Evolution, Development and Functions F
journal, April 2013


S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
journal, June 2002


A 25-Amino Acid Sequence of the Arabidopsis TGD2 Protein Is Sufficient for Specific Binding of Phosphatidic Acid
journal, May 2009


Profiling Membrane Lipids in Plant Stress Responses: ROLE OF PHOSPHOLIPASE Dα IN FREEZING-INDUCED LIPID CHANGES IN
journal, June 2002


Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering
journal, April 2014


Phloem-exudate proteome analysis of response to insect brown plant-hopper in rice
journal, July 2015


Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis
journal, January 2013


Overexpression of the Arabidopsis 10-Kilodalton Acyl-Coenzyme A-Binding Protein ACBP6 Enhances Freezing Tolerance
journal, July 2008


Phloem small RNAs, nutrient stress responses, and systemic mobility
journal, January 2010


Characterisation of microRNAs from apple (Malus domestica 'Royal Gala') vascular tissue and phloem sap
journal, January 2010


Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.)
journal, January 2011


Secretome Analysis Reveals an Arabidopsis Lipase Involved in Defense against Alternaria brassicicola
journal, August 2005


Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis
journal, March 2002


Symplasmic protein and RNA traffic: regulatory points and regulatory factors
journal, December 2003


Protein profile of Lupinus texensis phloem sap exudates: Searching for Fe- and Zn-containing proteins
journal, July 2013


Surface structure and properties of plant seed oil bodies
journal, April 1992


Phosphatidylinositol 4,5-Bisphosphate Influences PIN Polarization by Controlling Clathrin-Mediated Membrane Trafficking in Arabidopsis
journal, December 2013


Proteome study of the phloem sap of pumpkin using multidimensional protein identification technology
journal, July 2010


Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse
journal, January 2000


Hormonal regulation of tomato gibberellin 20-oxidase1 expressed in Arabidopsis
journal, September 2010


A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking
journal, July 2006


The broccoli (Brassica oleracea) phloem tissue proteome
journal, January 2013


Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants
journal, October 1999


Works referencing / citing this record:

Vascular Sap Proteomics: Providing Insight into Long-Distance Signaling during Stress
journal, May 2016


Vascular Sap Proteomics: Providing Insight into Long-Distance Signaling during Stress
journal, May 2016


Depletion of Arabidopsis ACYL-COA-BINDING PROTEIN3 Affects Fatty Acid Composition in the Phloem
journal, January 2018