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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

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 » 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.« less

Authors:
ORCiD logo; ;
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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.bbalip.2016.01.022

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Cited by: 7 works
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Works referencing / citing this record:

Evolutionary Diversification of Primary Metabolism and Its Contribution to Plant Chemical Diversity
journal, July 2019