skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mouse fat storage-inducing transmembrane protein 2 (FIT2) promotes lipid droplet accumulation in plants

Abstract

Fat storage-inducing transmembrane protein 2 (FIT2) is an endoplasmic reticulum (ER)-localized protein that plays an important role in lipid droplet (LD) formation in animal cells. However, no obvious homologue of FIT2 is found in plants. We tested the function of FIT2 in plant cells by ectopically expressing mouse (Mus musculus) FIT2 in Nicotiana tabacum suspension-cultured cells, Nicotiana benthamiana leaves and Arabidopsis thaliana plants. Confocal microscopy indicated that the expression of FIT2 dramatically increased the number and size of LDs in leaves of N. benthamiana and Arabidopsis, and lipidomics analysis and mass spectrometry imaging confirmed the accumulation of neutral lipids in leaves. FIT2 also increased seed oil content by ~13% in some stable, overexpressing lines of Arabidopsis. Furthermore, when expressed transiently in leaves of N. benthamiana or suspension cells of N. tabacum, FIT2 localized specifically to the ER and was often concentrated at certain regions of the ER that resembled ER-LD junction sites. FIT2 also colocalized at the ER with other proteins known to be involved in triacylglycerol biosynthesis or LD formation in plants, but not with ER resident proteins involved in electron transfer or ERvesicle exit sites. Collectively, these results demonstrate that mouse FIT2 promotes LD accumulation in plants, amore » surprising functional conservation in the context of a plant cell given the apparent lack of FIT2 homologues in higher plants. Our results suggest also that FIT2 expression represents an effective synthetic biology strategy for elaborating neutral lipid compartments in plant tissues for potential biofuel or bioproduct purposes.« less

Authors:
 [1];  [1];  [1];  [2];  [2];  [2];  [3];  [3];  [1];  [2];  [3];  [1]
  1. Center for Plant Lipid Research, University of North Texas, Denton TX USA
  2. Department of Molecular and Cellular Biology, University of Guelph, Guelph ON Canada
  3. US Arid-Land Agricultural Research Center, USDA-ARS, Maricopa AZ USA
Publication Date:
Research Org.:
Univ. of North Texas, Denton, TX (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Natural Sciences and Engineering Research Council of Canada (NSERC)
OSTI Identifier:
1339585
Alternate Identifier(s):
OSTI ID: 1339586; OSTI ID: 1374537
Grant/Contract Number:  
SC0016536; FG02-09ER64812
Resource Type:
Published Article
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Name: Plant Biotechnology Journal Journal Volume: 15 Journal Issue: 7; Journal ID: ISSN 1467-7644
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; endoplasmic reticulum; fat storage-inducing transmembrane protein 2; lipid droplets; lipid storage; triacylglycerol; lipid partitioning

Citation Formats

Cai, Yingqi, McClinchie, Elizabeth, Price, Ann, Nguyen, Thuy N., Gidda, Satinder K., Watt, Samantha C., Yurchenko, Olga, Park, Sunjung, Sturtevant, Drew, Mullen, Robert T., Dyer, John M., and Chapman, Kent D. Mouse fat storage-inducing transmembrane protein 2 (FIT2) promotes lipid droplet accumulation in plants. United Kingdom: N. p., 2017. Web. doi:10.1111/pbi.12678.
Cai, Yingqi, McClinchie, Elizabeth, Price, Ann, Nguyen, Thuy N., Gidda, Satinder K., Watt, Samantha C., Yurchenko, Olga, Park, Sunjung, Sturtevant, Drew, Mullen, Robert T., Dyer, John M., & Chapman, Kent D. Mouse fat storage-inducing transmembrane protein 2 (FIT2) promotes lipid droplet accumulation in plants. United Kingdom. doi:10.1111/pbi.12678.
Cai, Yingqi, McClinchie, Elizabeth, Price, Ann, Nguyen, Thuy N., Gidda, Satinder K., Watt, Samantha C., Yurchenko, Olga, Park, Sunjung, Sturtevant, Drew, Mullen, Robert T., Dyer, John M., and Chapman, Kent D. Wed . "Mouse fat storage-inducing transmembrane protein 2 (FIT2) promotes lipid droplet accumulation in plants". United Kingdom. doi:10.1111/pbi.12678.
@article{osti_1339585,
title = {Mouse fat storage-inducing transmembrane protein 2 (FIT2) promotes lipid droplet accumulation in plants},
author = {Cai, Yingqi and McClinchie, Elizabeth and Price, Ann and Nguyen, Thuy N. and Gidda, Satinder K. and Watt, Samantha C. and Yurchenko, Olga and Park, Sunjung and Sturtevant, Drew and Mullen, Robert T. and Dyer, John M. and Chapman, Kent D.},
abstractNote = {Fat storage-inducing transmembrane protein 2 (FIT2) is an endoplasmic reticulum (ER)-localized protein that plays an important role in lipid droplet (LD) formation in animal cells. However, no obvious homologue of FIT2 is found in plants. We tested the function of FIT2 in plant cells by ectopically expressing mouse (Mus musculus) FIT2 in Nicotiana tabacum suspension-cultured cells, Nicotiana benthamiana leaves and Arabidopsis thaliana plants. Confocal microscopy indicated that the expression of FIT2 dramatically increased the number and size of LDs in leaves of N. benthamiana and Arabidopsis, and lipidomics analysis and mass spectrometry imaging confirmed the accumulation of neutral lipids in leaves. FIT2 also increased seed oil content by ~13% in some stable, overexpressing lines of Arabidopsis. Furthermore, when expressed transiently in leaves of N. benthamiana or suspension cells of N. tabacum, FIT2 localized specifically to the ER and was often concentrated at certain regions of the ER that resembled ER-LD junction sites. FIT2 also colocalized at the ER with other proteins known to be involved in triacylglycerol biosynthesis or LD formation in plants, but not with ER resident proteins involved in electron transfer or ERvesicle exit sites. Collectively, these results demonstrate that mouse FIT2 promotes LD accumulation in plants, a surprising functional conservation in the context of a plant cell given the apparent lack of FIT2 homologues in higher plants. Our results suggest also that FIT2 expression represents an effective synthetic biology strategy for elaborating neutral lipid compartments in plant tissues for potential biofuel or bioproduct purposes.},
doi = {10.1111/pbi.12678},
journal = {Plant Biotechnology Journal},
number = 7,
volume = 15,
place = {United Kingdom},
year = {2017},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1111/pbi.12678

Citation Metrics:
Cited by: 4 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Seed-Development Programs: A Systems Biology–Based Comparison Between Dicots and Monocots
journal, April 2013


Structural Insights into Triglyceride Storage Mediated by Fat Storage-Inducing Transmembrane (FIT) Protein 2
journal, May 2010


Oil bodies and their associated proteins, oleosin and caleosin
journal, July 2001


Endoplasmic Reticulum, Oleosins, and Oils in Seeds and Tapetum Cells
journal, November 2004


Arabidopsis SEIPIN Proteins Modulate Triacylglycerol Accumulation and Influence Lipid Droplet Proliferation
journal, September 2015

  • Cai, Yingqi; Goodman, Joel M.; Pyc, Michal
  • The Plant Cell, Vol. 27, Issue 9
  • DOI: 10.1105/tpc.15.00588

The α/β Hydrolase CGI-58 and Peroxisomal Transport Protein PXA1 Coregulate Lipid Homeostasis and Signaling in Arabidopsis
journal, May 2013

  • Park, Sunjung; Gidda, Satinder K.; James, Christopher N.
  • The Plant Cell, Vol. 25, Issue 5, p. 1726-1739
  • DOI: 10.1105/tpc.113.111898

Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae
journal, June 2011

  • Jacquier, N.; Choudhary, V.; Mari, M.
  • Journal of Cell Science, Vol. 124, Issue 14
  • DOI: 10.1242/jcs.076836

Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A Cooperate in Cell Cycle–Associated Replication of Peroxisomes
journal, June 2008

  • Lingard, Matthew J.; Gidda, Satinder K.; Bingham, Scott
  • The Plant Cell, Vol. 20, Issue 6
  • DOI: 10.1105/tpc.107.057679

Biogenesis of the multifunctional lipid droplet: Lipids, proteins, and sites
journal, March 2014

  • Pol, Albert; Gross, Steven P.; Parton, Robert G.
  • The Journal of Cell Biology, Vol. 204, Issue 5
  • DOI: 10.1083/jcb.201311051

Seipin is required for converting nascent to mature lipid droplets
journal, August 2016


The dynamic roles of intracellular lipid droplets: from archaea to mammals
journal, October 2011


Compartmentation of Triacylglycerol Accumulation in Plants
journal, November 2011

  • Chapman, Kent D.; Ohlrogge, John B.
  • Journal of Biological Chemistry, Vol. 287, Issue 4, p. 2288-2294
  • DOI: 10.1074/jbc.R111.290072

Heterologous expression of AtClo1, a plant oil body protein, induces lipid accumulation in yeast
journal, May 2009


PERILIPIN-Dependent Control of Lipid Droplet Structure and Fat Storage in Drosophila
journal, November 2010


Rapid expression of transgenes driven by seed-specific constructs in leaf tissue: DHA production
journal, January 2010

  • Petrie, James R.; Shrestha, Pushkar; Liu, Qing
  • Plant Methods, Vol. 6, Issue 1
  • DOI: 10.1186/1746-4811-6-8

Novel Targeting Signals Mediate the Sorting of Different Isoforms of the Tail-Anchored Membrane Protein Cytochrome b 5 to Either Endoplasmic Reticulum or Mitochondria
journal, October 2004

  • Hwang, Yeen Ting; Pelitire, Scott M.; Henderson, Matthew P. A.
  • The Plant Cell, Vol. 16, Issue 11
  • DOI: 10.1105/tpc.104.026039

LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves
journal, August 2005


Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation
journal, November 2011

  • Gross, D. A.; Zhan, C.; Silver, D. L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 49
  • DOI: 10.1073/pnas.1110817108

Spatial Mapping of Lipids at Cellular Resolution in Embryos of Cotton
journal, February 2012

  • Horn, Patrick J.; Korte, Andrew R.; Neogi, Purnima B.
  • The Plant Cell, Vol. 24, Issue 2
  • DOI: 10.1105/tpc.111.094581

In Vivo Packaging of Triacylglycerols Enhances Arabidopsis Leaf Biomass and Energy Density
journal, April 2013

  • Winichayakul, Somrutai; Scott, Richard William; Roldan, Marissa
  • Plant Physiology, Vol. 162, Issue 2
  • DOI: 10.1104/pp.113.216820

Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum
journal, September 2013

  • Jacquier, N.; Mishra, S.; Choudhary, V.
  • Journal of Cell Science, Vol. 126, Issue 22
  • DOI: 10.1242/jcs.131896

Lipid Droplets Finally Get a Little R-E-S-P-E-C-T
journal, November 2009


A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta
journal, September 2003

  • Curtis, Mark D.; Grossniklaus, Ueli
  • Plant Physiology, Vol. 133, Issue 2, p. 462-469
  • DOI: 10.1104/pp.103.027979

Expression of perilipin 5 promotes lipid droplet formation in yeast
journal, August 2015


Mature lipid droplets are accessible to ER luminal proteins
journal, September 2016

  • Mishra, Shirish; Khaddaj, Rasha; Cottier, Stéphanie
  • Journal of Cell Science, Vol. 129, Issue 20
  • DOI: 10.1242/jcs.189191

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

  • Welti, Ruth; Li, Weiqi; Li, Maoyin
  • Journal of Biological Chemistry, Vol. 277, Issue 35
  • DOI: 10.1074/jbc.M205375200

Identification of a New Class of Lipid Droplet-Associated Proteins in Plants
journal, July 2013

  • Horn, Patrick J.; James, Christopher N.; Gidda, Satinder K.
  • Plant Physiology, Vol. 162, Issue 4
  • DOI: 10.1104/pp.113.222455

Formation of stacked ER cisternae by low affinity protein interactions
journal, October 2003

  • Snapp, Erik L.; Hegde, Ramanujan S.; Francolini, Maura
  • The Journal of Cell Biology, Vol. 163, Issue 2
  • DOI: 10.1083/jcb.200306020

Conserved Amphipathic Helices Mediate Lipid Droplet Targeting of Perilipins 1–3
journal, January 2016

  • Rowe, Emily R.; Mimmack, Michael L.; Barbosa, Antonio D.
  • Journal of Biological Chemistry, Vol. 291, Issue 13
  • DOI: 10.1074/jbc.M115.691048

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

Lipid droplet biogenesis
journal, August 2014

  • Wilfling, Florian; Haas, Joel T.; Walther, Tobias C.
  • Current Opinion in Cell Biology, Vol. 29
  • DOI: 10.1016/j.ceb.2014.03.008

Disruption of the Arabidopsis CGI-58 homologue produces Chanarin–Dorfman-like lipid droplet accumulation in plants
journal, September 2010

  • James, Christopher N.; Horn, Patrick J.; Case, Charlene R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 41, p. 17833-17838
  • DOI: 10.1073/pnas.0911359107

When Proteomics Reveals Unsuspected Roles: The Plastoglobule Example
journal, January 2013


Hydrophobic-Domain-Dependent Protein-Protein Interactions Mediate the Localization of GPAT Enzymes to ER Subdomains
journal, February 2011


The life of lipid droplets
journal, June 2009

  • Walther, Tobias C.; Farese, Robert V.
  • Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 6
  • DOI: 10.1016/j.bbalip.2008.10.009

Fat Storage-inducing Transmembrane Protein 2 Is Required for Normal Fat Storage in Adipose Tissue
journal, February 2014

  • Miranda, Diego A.; Kim, Ji-Hyun; Nguyen, Long N.
  • Journal of Biological Chemistry, Vol. 289, Issue 14
  • DOI: 10.1074/jbc.M114.547687

A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
journal, July 1962


Packaging of Fat: An Evolving Model of Lipid Droplet Assembly and Expansion
journal, November 2011

  • Brasaemle, Dawn L.; Wolins, Nathan E.
  • Journal of Biological Chemistry, Vol. 287, Issue 4
  • DOI: 10.1074/jbc.R111.309088

The lipid droplet—a well-connected organelle
journal, August 2015


The ontogeny of lipid bodies (spherosomes) in plant cells: Ultrastructural evidence
journal, February 1981

  • Wanner, G.; Formanek, H.; Theimer, R. R.
  • Planta, Vol. 151, Issue 2
  • DOI: 10.1007/BF00387812

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


Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis
journal, October 2006

  • Robenek, H.; Hofnagel, O.; Buers, I.
  • Journal of Cell Science, Vol. 119, Issue 20
  • DOI: 10.1242/jcs.03191

The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology
journal, December 2007

  • Szymanski, K. M.; Binns, D.; Bartz, R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 52
  • DOI: 10.1073/pnas.0704154104

Lipidomics in situ: Insights into plant lipid metabolism from high resolution spatial maps of metabolites
journal, April 2014


A conserved family of proteins facilitates nascent lipid droplet budding from the ER
journal, October 2015

  • Choudhary, Vineet; Ojha, Namrata; Golden, Andy
  • The Journal of Cell Biology, Vol. 211, Issue 2
  • DOI: 10.1083/jcb.201505067

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


LipidomeDB Data Calculation Environment: Online Processing of Direct-Infusion Mass Spectral Data for Lipid Profiles
journal, June 2011


Postnatal Deletion of Fat Storage-inducing Transmembrane Protein 2 (FIT2/FITM2) Causes Lethal Enteropathy
journal, August 2015

  • Goh, Vera J.; Tan, Jolene S. Y.; Tan, Bryan C.
  • Journal of Biological Chemistry, Vol. 290, Issue 42
  • DOI: 10.1074/jbc.M115.676700

Transcriptional transitions in Nicotiana benthamiana leaves upon induction of oil synthesis by WRINKLED1 homologs from diverse species and tissues
journal, August 2015


Quantitative profiling and pattern analysis of triacylglycerol species in Arabidopsis seeds by electrospray ionization mass spectrometry
journal, November 2013

  • Li, Maoyin; Baughman, Ethan; Roth, Mary R.
  • The Plant Journal, Vol. 77, Issue 1
  • DOI: 10.1111/tpj.12365

Biogenesis and functions of lipid droplets in plants: Thematic Review Series: Lipid Droplet Synthesis and Metabolism: from Yeast to Man
journal, November 2011

  • Chapman, Kent D.; Dyer, John M.; Mullen, Robert T.
  • Journal of Lipid Research, Vol. 53, Issue 2
  • DOI: 10.1194/jlr.R021436

Synergistic effect of WRI1 and DGAT1 coexpression on triacylglycerol biosynthesis in plants
journal, January 2013


Plastoglobules Are Lipoprotein Subcompartments of the Chloroplast That Are Permanently Coupled to Thylakoid Membranes and Contain Biosynthetic Enzymes
journal, May 2006

  • Austin, Jotham R.; Frost, Elizabeth; Vidi, Pierre-Alexandre
  • The Plant Cell, Vol. 18, Issue 7
  • DOI: 10.1105/tpc.105.039859

The plant lipidome in human and environmental health
journal, September 2016


Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways
journal, September 2009


Oleosins and Oil Bodies in Seeds and Other Organs
journal, April 1996


Tobacco as a production platform for biofuel overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass
journal, April 2010


Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells
journal, September 2007


Reduced Oil Accumulation in Cottonseeds Transformed with a Nonfunctional Allele of a Delta-12 Fatty Acid Desaturase ()
journal, January 2008


Metabolite Imager: customized spatial analysis of metabolite distributions in mass spectrometry imaging
journal, August 2013


LEAFY COTYLEDON1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis
journal, August 2008


Lipid Droplet-Associated Proteins (LDAPs) Are Required for the Dynamic Regulation of Neutral Lipid Compartmentation in Plant Cells
journal, February 2016

  • Gidda, Satinder K.; Park, Sunjung; Pyc, Michal
  • Plant Physiology, Vol. 170, Issue 4
  • DOI: 10.1104/pp.15.01977

Tung Tree DGAT1 and DGAT2 Have Nonredundant Functions in Triacylglycerol Biosynthesis and Are Localized to Different Subdomains of the Endoplasmic Reticulum
journal, August 2006

  • Shockey, Jay M.; Gidda, Satinder K.; Chapital, Dorselyn C.
  • The Plant Cell, Vol. 18, Issue 9
  • DOI: 10.1105/tpc.106.043695

The biogenesis and functions of lipid bodies in animals, plants and microorganisms
journal, September 2001


Dynamic organization of COPII coat proteins at endoplasmic reticulum export sites in plant cells
journal, March 2009


Evolutionarily conserved gene family important for fat storage
journal, December 2007

  • Kadereit, B.; Kumar, P.; Wang, W. -J.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 1
  • DOI: 10.1073/pnas.0708579105

Altered Lipid Composition and Enhanced Nutritional Value of Arabidopsis Leaves following Introduction of an Algal Diacylglycerol Acyltransferase 2
journal, February 2013


Matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) for direct visualization of plant metabolites in situ
journal, February 2016


    Works referencing / citing this record:

    Mechanisms of lipid droplet biogenesis
    journal, July 2019

    • Chapman, Kent D.; Aziz, Mina; Dyer, John M.
    • Biochemical Journal, Vol. 476, Issue 13
    • DOI: 10.1042/bcj20180021

    Mechanisms of lipid droplet biogenesis
    journal, July 2019

    • Chapman, Kent D.; Aziz, Mina; Dyer, John M.
    • Biochemical Journal, Vol. 476, Issue 13
    • DOI: 10.1042/bcj20180021