How did nature engineer the highest surface lipid accumulation among plants? Exceptional expression of acyl-lipid-associated genes for the assembly of extracellular triacylglycerol by Bayberry (Myrica pensylvanica) fruits
Abstract
Bayberry (Myrica pensylvanica) fruits are covered with a remarkably thick layer of crystalline wax consisting of triacylglycerol (TAG) and diacylglycerol (DAG) esterified exclusively with saturated fatty acids. As the only plant known to accumulate soluble glycerolipids as a major component of surface waxes, Bayberry represents a novel system to investigate neutral lipid biosynthesis and lipid secretion by vegetative plant cells. The assembly of Bayberry wax is distinct from conventional TAG and other surface waxes, and instead proceeds through a pathway related to cutin synthesis (Simpson and Ohlrogge, 2016). In this study, microscopic examination revealed that the fruit tissue that produces and secretes wax (Bayberry knobs) is fully developed before wax accumulates and that wax is secreted to the surface without cell disruption. Comparison of transcript expression to genetically related tissues (Bayberry leaves, M. rubra fruits), cutin-rich tomato and cherry fruit epidermis, and to oil-rich mesocarp and seeds, revealed exceptionally high expression of 13 transcripts for acyl-lipid metabolism together with down-regulation of fatty acid oxidases and desaturases. The predicted protein sequences of the most highly expressed lipid-related enzyme-encoding transcripts in Bayberry knobs are 100% identical to the sequences from Bayberry leaves,which do not produce surface DAG or TAG. Together, these resultsmore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1389694
- Alternate Identifier(s):
- OSTI ID: 1438200
- Grant/Contract Number:
- BER DE-FC02-07ER64494; PGS-D3; FC02-07ER64494
- Resource Type:
- Published Article
- Journal Name:
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids
- Additional Journal Information:
- Journal Name: Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids Journal Volume: 1861 Journal Issue: 9 PB; Journal ID: ISSN 1388-1981
- Publisher:
- Elsevier
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Pathway evolution; Lipid secretion; Cuticle; Transacylase
Citation Formats
Simpson, Jeffrey P., Thrower, Nicholas, and Ohlrogge, John B. How did nature engineer the highest surface lipid accumulation among plants? Exceptional expression of acyl-lipid-associated genes for the assembly of extracellular triacylglycerol by Bayberry (Myrica pensylvanica) fruits. Netherlands: N. p., 2016.
Web. doi:10.1016/j.bbalip.2016.01.022.
Simpson, Jeffrey P., Thrower, Nicholas, & Ohlrogge, John B. How did nature engineer the highest surface lipid accumulation among plants? Exceptional expression of acyl-lipid-associated genes for the assembly of extracellular triacylglycerol by Bayberry (Myrica pensylvanica) fruits. Netherlands. https://doi.org/10.1016/j.bbalip.2016.01.022
Simpson, Jeffrey P., Thrower, Nicholas, and Ohlrogge, John B. Thu .
"How did nature engineer the highest surface lipid accumulation among plants? Exceptional expression of acyl-lipid-associated genes for the assembly of extracellular triacylglycerol by Bayberry (Myrica pensylvanica) fruits". Netherlands. https://doi.org/10.1016/j.bbalip.2016.01.022.
@article{osti_1389694,
title = {How did nature engineer the highest surface lipid accumulation among plants? Exceptional expression of acyl-lipid-associated genes for the assembly of extracellular triacylglycerol by Bayberry (Myrica pensylvanica) fruits},
author = {Simpson, Jeffrey P. and Thrower, Nicholas and Ohlrogge, John B.},
abstractNote = {Bayberry (Myrica pensylvanica) fruits are covered with a remarkably thick layer of crystalline wax consisting of triacylglycerol (TAG) and diacylglycerol (DAG) esterified exclusively with saturated fatty acids. As the only plant known to accumulate soluble glycerolipids as a major component of surface waxes, Bayberry represents a novel system to investigate neutral lipid biosynthesis and lipid secretion by vegetative plant cells. The assembly of Bayberry wax is distinct from conventional TAG and other surface waxes, and instead proceeds through a pathway related to cutin synthesis (Simpson and Ohlrogge, 2016). In this study, microscopic examination revealed that the fruit tissue that produces and secretes wax (Bayberry knobs) is fully developed before wax accumulates and that wax is secreted to the surface without cell disruption. Comparison of transcript expression to genetically related tissues (Bayberry leaves, M. rubra fruits), cutin-rich tomato and cherry fruit epidermis, and to oil-rich mesocarp and seeds, revealed exceptionally high expression of 13 transcripts for acyl-lipid metabolism together with down-regulation of fatty acid oxidases and desaturases. The predicted protein sequences of the most highly expressed lipid-related enzyme-encoding transcripts in Bayberry knobs are 100% identical to the sequences from Bayberry leaves,which do not produce surface DAG or TAG. Together, these results indicate that TAG biosynthesis and secretion in Bayberry is achieved by both up and down-regulation of a small subset of genes related to the biosynthesis of cutin and saturated fatty acids, and also implies that modifications in gene expression, rather than evolution of new gene functions, was the major mechanism by which Bayberry evolved its specialized lipid metabolism.},
doi = {10.1016/j.bbalip.2016.01.022},
journal = {Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids},
number = 9 PB,
volume = 1861,
place = {Netherlands},
year = {Thu Sep 01 00:00:00 EDT 2016},
month = {Thu Sep 01 00:00:00 EDT 2016}
}
https://doi.org/10.1016/j.bbalip.2016.01.022
Web of Science
Works referenced in this record:
The biosynthesis, composition and assembly of the outer pollen wall: A tough case to crack
journal, May 2015
- Quilichini, Teagen D.; Grienenberger, Etienne; Douglas, Carl J.
- Phytochemistry, Vol. 113
Tomato GDSL1 Is Required for Cutin Deposition in the Fruit Cuticle
journal, July 2012
- Girard, Anne-Laure; Mounet, Fabien; Lemaire-Chamley, Martine
- The Plant Cell, Vol. 24, Issue 7
A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol
journal, June 2010
- Yang, W.; Pollard, M.; Li-Beisson, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 26
Sealing Plant Surfaces: Cuticular Wax Formation by Epidermal Cells
journal, June 2008
- Samuels, Lacey; Kunst, Ljerka; Jetter, Reinhard
- Annual Review of Plant Biology, Vol. 59, Issue 1
Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid -hydroxylation in development
journal, August 2001
- Wellesen, K.; Durst, F.; Pinot, F.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 17
Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis
journal, June 2009
- Baud, Sébastien; Lepiniec, Loïc
- Plant Physiology and Biochemistry, Vol. 47, Issue 6
A Novel Pathway for Triacylglycerol Biosynthesis Is Responsible for the Accumulation of Massive Quantities of Glycerolipids in the Surface Wax of Bayberry ( Myrica pensylvanica ) Fruit
journal, January 2016
- Simpson, Jeffrey P.; Ohlrogge, John B.
- The Plant Cell, Vol. 28, Issue 1
Tissue fixation and staining with osmium tetroxide: the role of phenolic compounds.
journal, February 1978
- Nielson, A. J.; Griffith, W. P.
- Journal of Histochemistry & Cytochemistry, Vol. 26, Issue 2
Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers
journal, November 2007
- Li, Y.; Beisson, F.; Koo, A. J. K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 46
A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack
journal, July 2002
- Vailleau, F.; Daniel, X.; Tronchet, M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 15
Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells
journal, February 2008
- McFarlane, Heather E.; Young, Robin E.; Wasteneys, Geoffrey O.
- Planta, Vol. 227, Issue 6
Hydroxy and normal fatty acid distribution in stigmas of Nicotiana and other plants
journal, January 1988
- Koiwai, Kira; Matsuzaki, Toshiake
- Phytochemistry, Vol. 27, Issue 9
Following evolution's lead to a single residue switch for diterpene synthase product outcome
journal, April 2007
- Xu, M.; Wilderman, P. R.; Peters, R. J.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 18
The ABC Transporter ABCG1 Is Required for Suberin Formation in Potato Tuber Periderm
journal, August 2014
- Landgraf, Ramona; Smolka, Ulrike; Altmann, Simone
- The Plant Cell, Vol. 26, Issue 8
Living off the Wax of the Land: Bayberries and Yellow-Rumped Warblers
journal, April 1992
- Place, Allen R.; Stiles, Edmund W.
- The Auk, Vol. 109, Issue 2
Fatty Acid Metabolism
journal, June 1988
- Harwood, J. L.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 39, Issue 1
Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain α-,ω-dicarboxylic fatty acids and formation of extracellular matrix
journal, January 2006
- Kurdyukov, Sergey; Faust, Andrea; Trenkamp, Sandra
- Planta, Vol. 224, Issue 2
Solving the puzzles of cutin and suberin polymer biosynthesis
journal, June 2012
- Beisson, Fred; Li-Beisson, Yonghua; Pollard, Mike
- Current Opinion in Plant Biology, Vol. 15, Issue 3
Cuticular Lipid Composition, Surface Structure, and Gene Expression in Arabidopsis Stem Epidermis
journal, November 2005
- Suh, Mi Chung; Samuels, A. Lacey; Jetter, Reinhard
- Plant Physiology, Vol. 139, Issue 4
Toward production of jet fuel functionality in oilseeds: identification of FatB acyl-acyl carrier protein thioesterases and evaluation of combinatorial expression strategies in Camelina seeds
journal, May 2015
- Kim, Hae Jin; Silva, Jillian E.; Vu, Hieu Sy
- Journal of Experimental Botany, Vol. 66, Issue 14
Disruption of the FATB Gene in Arabidopsis Demonstrates an Essential Role of Saturated Fatty Acids in Plant Growth
journal, March 2003
- Bonaventure, Gustavo; Salas, Joaquin J.; Pollard, Michael R.
- The Plant Cell, Vol. 15, Issue 4
The evolutionary paths towards complexity: a metabolic perspective
journal, July 2013
- Weng, Jing-Ke
- New Phytologist, Vol. 201, Issue 4
Transcriptomic analysis of Chinese bayberry (Myrica rubra) fruit development and ripening using RNA-Seq
journal, January 2012
- Feng, Chao; Chen, Ming; Xu, Chang-jie
- BMC Genomics, Vol. 13, Issue 1
Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants
journal, February 2014
- Yeats, Trevor H.; Huang, Wenlin; Chatterjee, Subhasish
- The Plant Journal, Vol. 77, Issue 5
The Arabidopsis DCR Encoding a Soluble BAHD Acyltransferase Is Required for Cutin Polyester Formation and Seed Hydration Properties
journal, October 2009
- Panikashvili, David; Shi, Jian Xin; Schreiber, Lukas
- Plant Physiology, Vol. 151, Issue 4
A MYB Transcription Factor Regulates Very-Long-Chain Fatty Acid Biosynthesis for Activation of the Hypersensitive Cell Death Response in Arabidopsis
journal, March 2008
- Raffaele, Sylvain; Vailleau, Fabienne; Léger, Amandine
- The Plant Cell, Vol. 20, Issue 3
Identification of a Lipid Transfer Protein as the Major Protein in the Surface Wax of Broccoli (Brassica oleracea) Leaves
journal, June 1994
- Pyee, J.; Yu, H. S.; Kolattukudy, P. E.
- Archives of Biochemistry and Biophysics, Vol. 311, Issue 2
Changes in Stigma-Specific Lipids of Tobacco Plant during Flower Development
journal, January 1983
- Matsuzaki, T.; Koiwai, A.; Kawashima, N.
- Plant and Cell Physiology, Vol. 24, Issue 2
Acyl-Lipid Metabolism
journal, January 2013
- Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred
- The Arabidopsis Book, Vol. 11
The Transcription Factor WIN1/SHN1 Regulates Cutin Biosynthesis in Arabidopsis thaliana
journal, April 2007
- Kannangara, Rubini; Branigan, Caroline; Liu, Yan
- The Plant Cell, Vol. 19, Issue 4
AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types
journal, August 2014
- Kosma, Dylan K.; Murmu, Jhadeswar; Razeq, Fakhria M.
- The Plant Journal, Vol. 80, Issue 2
WRI1 Is Required for Seed Germination and Seedling Establishment
journal, June 2006
- Cernac, Alex; Andre, Carl; Hoffmann-Benning, Susanne
- Plant Physiology, Vol. 141, Issue 2, p. 745-757
Role of HXXXD-motif/BAHD acyltransferases in the biosynthesis of extracellular lipids
journal, December 2014
- Molina, Isabel; Kosma, Dylan
- Plant Cell Reports, Vol. 34, Issue 4
The identification of cutin synthase: formation of the plant polyester cutin
journal, May 2012
- Yeats, Trevor H.; Martin, Laetitia B. B.; Viart, Hélène M-F
- Nature Chemical Biology, Vol. 8, Issue 7
A Nodule-Specific Lipid Transfer Protein AsE246 Participates in Transport of Plant-Synthesized Lipids to Symbiosome Membrane and Is Essential for Nodule Organogenesis in Chinese Milk Vetch
journal, December 2013
- Lei, Lei; Chen, Ling; Shi, Xiaofeng
- Plant Physiology, Vol. 164, Issue 2
Disruption of Glycosylphosphatidylinositol-Anchored Lipid Transfer Protein Gene Altered Cuticular Lipid Composition, Increased Plastoglobules, and Enhanced Susceptibility to Infection by the Fungal Pathogen Alternaria brassicicola
journal, March 2009
- Lee, Saet Buyl; Go, Young Sam; Bae, Hyun-Jong
- Plant Physiology, Vol. 150, Issue 1
Tapetal Origin of Pollen-Coat Substances in Lilium
journal, October 1968
- Heslop-Harrison, J.
- New Phytologist, Vol. 67, Issue 4
Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester
journal, December 2009
- Li-Beisson, Y.; Pollard, M.; Sauveplane, V.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 51
The Cytochrome P450 CYP86A22 Is a Fatty Acyl-CoA ω-Hydroxylase Essential for Estolide Synthesis in the Stigma of Petunia hybrida
journal, February 2010
- Han, Jixiang; Clement, Joel M.; Li, Jia
- Journal of Biological Chemistry, Vol. 285, Issue 6
Lipid-Transfer Proteins in Plants
journal, June 1996
- Kader, Jean-Claude
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Oil biosynthesis in a basal angiosperm: transcriptome analysis of Persea Americana mesocarp
journal, August 2015
- Kilaru, Aruna; Cao, Xia; Dabbs, Parker B.
- BMC Plant Biology, Vol. 15, Issue 1
WRINKLED Transcription Factors Orchestrate Tissue-Specific Regulation of Fatty Acid Biosynthesis in Arabidopsis
journal, December 2012
- To, Alexandra; Joubès, Jérôme; Barthole, Guillaume
- The Plant Cell, Vol. 24, Issue 12
Tissue-Specific Expression of a Gene Encoding a Cell Wall-Localized Lipid Transfer Protein from Arabidopsis
journal, May 1994
- Thoma, S.; Hecht, U.; Kippers, A.
- Plant Physiology, Vol. 105, Issue 1
Plant cell wall secretion and lipid traffic at membrane contact sites of the cell cortex
journal, December 2011
- Samuels, Lacey; McFarlane, Heather E.
- Protoplasma, Vol. 249, Issue S1
ABCG Transporters Are Required for Suberin and Pollen Wall Extracellular Barriers in Arabidopsis
journal, September 2014
- Yadav, V.; Molina, I.; Ranathunge, K.
- The Plant Cell, Vol. 26, Issue 9
The triglyceride composition of Myrica carolinensis fruit coat fat (bayberry tallow)
journal, September 1965
- Harlow, R. D.; Litchfield, Carter; Fu, Hwei-Choung
- Journal of the American Oil Chemists' Society, Vol. 42, Issue 9
Tissue- and Cell-Type Specific Transcriptome Profiling of Expanding Tomato Fruit Provides Insights into Metabolic and Regulatory Specialization and Cuticle Formation
journal, November 2011
- Matas, Antonio J.; Yeats, Trevor H.; Buda, Gregory J.
- The Plant Cell, Vol. 23, Issue 11
Transcriptional dynamics of the developing sweet cherry (Prunus avium L.) fruit: sequencing, annotation and expression profiling of exocarp-associated genes
journal, March 2014
- Alkio, Merianne; Jonas, Uwe; Declercq, Myriam
- Horticulture Research, Vol. 1, Issue 1
The SHINE Clade of AP2 Domain Transcription Factors Activates Wax Biosynthesis, Alters Cuticle Properties, and Confers Drought Tolerance when Overexpressed in Arabidopsis
journal, August 2004
- Aharoni, Asaph; Dixit, Shital; Jetter, Reinhard
- The Plant Cell, Vol. 16, Issue 9
Monoacylglycerols Are Components of Root Waxes and Can Be Produced in the Aerial Cuticle by Ectopic Expression of a Suberin-Associated Acyltransferase
journal, May 2007
- Li, Yonghua; Beisson, Fred; Ohlrogge, John
- Plant Physiology, Vol. 144, Issue 3
Tobacco NtLTP1, a glandular-specific lipid transfer protein, is required for lipid secretion from glandular trichomes: NtLTP1 involved in glandular trichome secretion
journal, February 2012
- Choi, Yong Eui; Lim, Soon; Kim, Hyun-Jung
- The Plant Journal, Vol. 70, Issue 3
Analysis of commercial waxes using capillary supercritical fluid chromatography—mass spectrometry
journal, January 1987
- Hawthorne, Steven B.; Miller, David J.
- Journal of Chromatography A, Vol. 388
Lipid extraction of tissues with a low-toxicity solvent
journal, October 1978
- Hara, Atsushi; Radin, Norman S.
- Analytical Biochemistry, Vol. 90, Issue 1
Knitting a polyester skin
journal, June 2012
- Beisson, Fred; Ohlrogge, John
- Nature Chemical Biology, Vol. 8, Issue 7
Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning
journal, June 2011
- Bourgis, F.; Kilaru, A.; Cao, X.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
Correlation of mRNA and protein abundance in the developing maize leaf
journal, April 2014
- Ponnala, Lalit; Wang, Yupeng; Sun, Qi
- The Plant Journal, Vol. 78, Issue 3
Arabidopsis LTPG Is a Glycosylphosphatidylinositol-Anchored Lipid Transfer Protein Required for Export of Lipids to the Plant Surface
journal, April 2009
- DeBono, Allan; Yeats, Trevor H.; Rose, Jocelyn K. C.
- The Plant Cell, Vol. 21, Issue 4
Works referencing / citing this record:
Evolutionary Diversification of Primary Metabolism and Its Contribution to Plant Chemical Diversity
journal, July 2019
- Maeda, Hiroshi A.
- Frontiers in Plant Science, Vol. 10