DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mobilizing Vacuolar Sugar Increases Vegetative Triacylglycerol Accumulation

Abstract

Photosynthetically derived sugars provide carbon skeletons for metabolism and carbon signals that favor anabolism. The amount of sugar available for fatty acid (FA) and triacylglycerol (TAG) synthesis depends on sugar compartmentation, transport, and demands from competing pathways. We are exploring the influence of sugar partitioning between the vacuole and cytoplasm on FA synthesis in Arabidopsis by building on our previous finding that reduced leaf sugar export in the sucrose-proton symporter2 (suc2) mutant, in combination with impaired starch synthesis in the ADP-glucose pyrophosphorylase (adg1) mutant, accumulates higher sugar levels and increased total FA and TAG compared to the wild type parent. Here we sought to relocalize sugar from the vacuole to the cytoplasm to drive additional FA/TAG synthesis and growth. Arabidopsis suc2 adg1 was therefore crossed with tonoplast monosaccharide transporter mutants tmt1 and tmt2 and overexpression of the sucrose/proton cotransporter SUC4 in which tmt1 tmt2 impairs sugar transport to the vacuole from the cytoplasm and SUC4 overexpression enhances sugar transport in the reverse direction from the vacuole to the cytoplasm. A resulting homozygous suc2 adg1 tmt1 tmt2 SUC4 line was used to test the hypothesis that increased intracellular carbon supply in the form of sugars would increase both FA and TAGmore » accumulation. The data shows that relative to suc2 adg1, suc2 adg1 tmt1 tmt2 SUC4 significantly increases leaf total FA content by 1.29-fold to 10.9% of dry weight and TAG by 2.4-fold to 2.88%, supporting the hypothesis that mobilizing vacuolar sugar is a valid strategy for increasing vegetative oil accumulation.« less

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [1]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1807933
Report Number(s):
BNL-221769-2021-JAAM
Journal ID: ISSN 1664-462X
Grant/Contract Number:  
SC0012704; SC0018254; KC0304000
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 12; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; triacylglycerol; fatty; acid; synthesis; sugar flux; sugar compartmentalization

Citation Formats

Anaokar, Sanket, Liu, Hui, Keereetaweep, Jantana, Zhai, Zhiyang, and Shanklin, John. Mobilizing Vacuolar Sugar Increases Vegetative Triacylglycerol Accumulation. United States: N. p., 2021. Web. doi:10.3389/fpls.2021.708902.
Anaokar, Sanket, Liu, Hui, Keereetaweep, Jantana, Zhai, Zhiyang, & Shanklin, John. Mobilizing Vacuolar Sugar Increases Vegetative Triacylglycerol Accumulation. United States. https://doi.org/10.3389/fpls.2021.708902
Anaokar, Sanket, Liu, Hui, Keereetaweep, Jantana, Zhai, Zhiyang, and Shanklin, John. Thu . "Mobilizing Vacuolar Sugar Increases Vegetative Triacylglycerol Accumulation". United States. https://doi.org/10.3389/fpls.2021.708902. https://www.osti.gov/servlets/purl/1807933.
@article{osti_1807933,
title = {Mobilizing Vacuolar Sugar Increases Vegetative Triacylglycerol Accumulation},
author = {Anaokar, Sanket and Liu, Hui and Keereetaweep, Jantana and Zhai, Zhiyang and Shanklin, John},
abstractNote = {Photosynthetically derived sugars provide carbon skeletons for metabolism and carbon signals that favor anabolism. The amount of sugar available for fatty acid (FA) and triacylglycerol (TAG) synthesis depends on sugar compartmentation, transport, and demands from competing pathways. We are exploring the influence of sugar partitioning between the vacuole and cytoplasm on FA synthesis in Arabidopsis by building on our previous finding that reduced leaf sugar export in the sucrose-proton symporter2 (suc2) mutant, in combination with impaired starch synthesis in the ADP-glucose pyrophosphorylase (adg1) mutant, accumulates higher sugar levels and increased total FA and TAG compared to the wild type parent. Here we sought to relocalize sugar from the vacuole to the cytoplasm to drive additional FA/TAG synthesis and growth. Arabidopsis suc2 adg1 was therefore crossed with tonoplast monosaccharide transporter mutants tmt1 and tmt2 and overexpression of the sucrose/proton cotransporter SUC4 in which tmt1 tmt2 impairs sugar transport to the vacuole from the cytoplasm and SUC4 overexpression enhances sugar transport in the reverse direction from the vacuole to the cytoplasm. A resulting homozygous suc2 adg1 tmt1 tmt2 SUC4 line was used to test the hypothesis that increased intracellular carbon supply in the form of sugars would increase both FA and TAG accumulation. The data shows that relative to suc2 adg1, suc2 adg1 tmt1 tmt2 SUC4 significantly increases leaf total FA content by 1.29-fold to 10.9% of dry weight and TAG by 2.4-fold to 2.88%, supporting the hypothesis that mobilizing vacuolar sugar is a valid strategy for increasing vegetative oil accumulation.},
doi = {10.3389/fpls.2021.708902},
journal = {Frontiers in Plant Science},
number = ,
volume = 12,
place = {United States},
year = {2021},
month = {8}
}

Works referenced in this record:

Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass
journal, June 2015

  • Zale, Janice; Jung, Je Hyeong; Kim, Jae Yoon
  • Plant Biotechnology Journal, Vol. 14, Issue 2
  • DOI: 10.1111/pbi.12411

The Mediator Complex MED15 Subunit Mediates Activation of Downstream Lipid-Related Genes by the WRINKLED1 Transcription Factor
journal, May 2016

  • Kim, Mi Jung; Jang, In-Cheol; Chua, Nam-Hai
  • Plant Physiology, Vol. 171, Issue 3
  • DOI: 10.1104/pp.16.00664

Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves
journal, October 2013

  • Vanhercke, Thomas; El Tahchy, Anna; Liu, Qing
  • Plant Biotechnology Journal, Vol. 12, Issue 2
  • DOI: 10.1111/pbi.12131

Sugar transport across the plant vacuolar membrane: nature and regulation of carrier proteins
journal, June 2015

  • Hedrich, Rainer; Sauer, Norbert; Neuhaus, H. Ekkehard
  • Current Opinion in Plant Biology, Vol. 25
  • DOI: 10.1016/j.pbi.2015.04.008

Dynamic and diverse sugar signaling
journal, October 2016


A Simple Method for Measuring the Starch and Lipid Contents in the Cell of Microalgae
journal, January 2015


Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2
journal, July 2011


Sugar Potentiation of Fatty Acid and Triacylglycerol Accumulation
journal, August 2017

  • Zhai, Zhiyang; Liu, Hui; Xu, Changcheng
  • Plant Physiology, Vol. 175, Issue 2
  • DOI: 10.1104/pp.17.00828

Tmt1: the first LTR-retrotransposon from a Tuber spp.
journal, October 2007


Step changes in leaf oil accumulation via iterative metabolic engineering
journal, January 2017


Sugar Transporters in Plants: New Insights and Discoveries
journal, June 2017

  • Julius, Benjamin T.; Leach, Kristen A.; Tran, Thu M.
  • Plant and Cell Physiology, Vol. 58, Issue 9
  • DOI: 10.1093/pcp/pcx090

Global Transcription Profiling Reveals Multiple Sugar Signal Transduction Mechanisms in Arabidopsis
journal, July 2004

  • Price, John; Laxmi, Ashverya; St. Martin, Steven K.
  • The Plant Cell, Vol. 16, Issue 8
  • DOI: 10.1105/tpc.104.022616

Triacylglycerol Metabolism, Function, and Accumulation in Plant Vegetative Tissues
journal, April 2016


On the Export of Fatty Acids from the Chloroplast
journal, February 2004

  • Koo, Abraham J. K.; Ohlrogge, John B.; Pollard, Mike
  • Journal of Biological Chemistry, Vol. 279, Issue 16
  • DOI: 10.1074/jbc.M311305200

The Role of Sugar Signaling in Regulating Plant Fatty Acid Synthesis
journal, March 2021


Molecular Identification and Physiological Characterization of a Novel Monosaccharide Transporter from Arabidopsis Involved in Vacuolar Sugar Transport
journal, December 2006

  • Wormit, Alexandra; Trentmann, Oliver; Feifer, Ingmar
  • The Plant Cell, Vol. 18, Issue 12
  • DOI: 10.1105/tpc.106.047290

Structure, evolution and diverse physiological roles of SWEET sugar transporters in plants
journal, April 2019

  • Jeena, Gajendra Singh; Kumar, Sunil; Shukla, Rakesh Kumar
  • Plant Molecular Biology, Vol. 100, Issue 4-5
  • DOI: 10.1007/s11103-019-00872-4

Starch Synthesis in Arabidopsis Is Achieved by Spatial Cotranscription of Core Starch Metabolism Genes
journal, September 2009

  • Tsai, Huang-Lung; Lue, Wei-Ling; Lu, Kuan-Jen
  • Plant Physiology, Vol. 151, Issue 3
  • DOI: 10.1104/pp.109.144196

Storing carbon in leaf lipid sinks enhances perennial ryegrass carbon capture especially under high N and elevated CO2
journal, November 2019

  • Beechey-Gradwell, Zac; Cooney, Luke; Winichayakul, Somrutai
  • Journal of Experimental Botany, Vol. 71, Issue 7
  • DOI: 10.1093/jxb/erz494

Increased Activity of the Vacuolar Monosaccharide Transporter TMT1 Alters Cellular Sugar Partitioning, Sugar Signaling, and Seed Yield in Arabidopsis
journal, August 2010

  • Wingenter, Karina; Schulz, Alexander; Wormit, Alexandra
  • Plant Physiology, Vol. 154, Issue 2
  • DOI: 10.1104/pp.110.162040