Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor

Thomas Vanhercke; Srinivas Belide; Matthew C. Taylor; Anna El Tahchy; Shoko Okada; Vivien Rolland; Qing Liu; Madeline Mitchell; Pushkar Shrestha; Ingrid Venables; Lina Ma; Cheryl Blundell; Anu Mathew; Lisa Ziolkowski; Nathalie Niesner; Dawar Hussain; Bei Dong; Guoquan Liu; Ian D. Godwin; Jiwon Lee; Melanie Rug; Xue Rong Zhou; Surinder P. Singh; James R. Petrie

doi:10.1111/pbi.12959

Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor

Thomas Vanhercke^*, Srinivas Belide, Matthew C. Taylor, Anna El Tahchy, Shoko Okada, Vivien Rolland, Qing Liu, Madeline Mitchell, Pushkar Shrestha, Ingrid Venables, Lina Ma, Cheryl Blundell, Anu Mathew, Lisa Ziolkowski, Nathalie Niesner, Dawar Hussain, Bei Dong, Guoquan Liu, Ian D. Godwin, Jiwon LeeMelanie Rug, Xue Rong Zhou, Surinder P. Singh, James R. Petrie

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

73 Citations (Scopus)

Abstract

Synthesis and accumulation of the storage lipid triacylglycerol in vegetative plant tissues has emerged as a promising strategy to meet the world's future need for vegetable oil. Sorghum (Sorghum bicolor) is a particularly attractive target crop given its high biomass, drought resistance and C ₄ photosynthesis. While oilseed-like triacylglycerol levels have been engineered in the C ₃ model plant tobacco, progress in C ₄ monocot crops has been lagging behind. In this study, we report the accumulation of triacylglycerol in sorghum leaf tissues to levels between 3 and 8.4% on a dry weight basis depending on leaf and plant developmental stage. This was achieved by the combined overexpression of genes encoding the Zea mays WRI1 transcription factor, Umbelopsis ramanniana UrDGAT2a acyltransferase and Sesamum indicum Oleosin-L oil body protein. Increased oil content was visible as lipid droplets, primarily in the leaf mesophyll cells. A comparison between a constitutive and mesophyll-specific promoter driving WRI1 expression revealed distinct changes in the overall leaf lipidome as well as transitory starch and soluble sugar levels. Metabolome profiling uncovered changes in the abundance of various amino acids and dicarboxylic acids. The results presented here are a first step forward towards the development of sorghum as a dedicated biomass oil crop and provide a basis for further combinatorial metabolic engineering.

Original language	English
Pages (from-to)	220-232
Number of pages	13
Journal	Plant Biotechnology Journal
Volume	17
Issue number	1
DOIs	https://doi.org/10.1111/pbi.12959
Publication status	Published - Jan 2019

Access to Document

10.1111/pbi.12959

Cite this

Vanhercke, T., Belide, S., Taylor, M. C., El Tahchy, A., Okada, S., Rolland, V., Liu, Q., Mitchell, M., Shrestha, P., Venables, I., Ma, L., Blundell, C., Mathew, A., Ziolkowski, L., Niesner, N., Hussain, D., Dong, B., Liu, G., Godwin, I. D., ... Petrie, J. R. (2019). Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor. Plant Biotechnology Journal, 17(1), 220-232. https://doi.org/10.1111/pbi.12959

@article{4c4f9ab519f146aea5fae1fd3690b6ad,

title = "Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor",

abstract = " Synthesis and accumulation of the storage lipid triacylglycerol in vegetative plant tissues has emerged as a promising strategy to meet the world's future need for vegetable oil. Sorghum (Sorghum bicolor) is a particularly attractive target crop given its high biomass, drought resistance and C 4 photosynthesis. While oilseed-like triacylglycerol levels have been engineered in the C 3 model plant tobacco, progress in C 4 monocot crops has been lagging behind. In this study, we report the accumulation of triacylglycerol in sorghum leaf tissues to levels between 3 and 8.4% on a dry weight basis depending on leaf and plant developmental stage. This was achieved by the combined overexpression of genes encoding the Zea mays WRI1 transcription factor, Umbelopsis ramanniana UrDGAT2a acyltransferase and Sesamum indicum Oleosin-L oil body protein. Increased oil content was visible as lipid droplets, primarily in the leaf mesophyll cells. A comparison between a constitutive and mesophyll-specific promoter driving WRI1 expression revealed distinct changes in the overall leaf lipidome as well as transitory starch and soluble sugar levels. Metabolome profiling uncovered changes in the abundance of various amino acids and dicarboxylic acids. The results presented here are a first step forward towards the development of sorghum as a dedicated biomass oil crop and provide a basis for further combinatorial metabolic engineering.",

keywords = "DGAT, Oleosin, Sorghum bicolor, WRI1, leaf, triacylglycerol",

author = "Thomas Vanhercke and Srinivas Belide and Taylor, {Matthew C.} and {El Tahchy}, Anna and Shoko Okada and Vivien Rolland and Qing Liu and Madeline Mitchell and Pushkar Shrestha and Ingrid Venables and Lina Ma and Cheryl Blundell and Anu Mathew and Lisa Ziolkowski and Nathalie Niesner and Dawar Hussain and Bei Dong and Guoquan Liu and Godwin, {Ian D.} and Jiwon Lee and Melanie Rug and Zhou, {Xue Rong} and Singh, {Surinder P.} and Petrie, {James R.}",

note = "Publisher Copyright: {\textcopyright} 2018 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.",

year = "2019",

month = jan,

doi = "10.1111/pbi.12959",

language = "English",

volume = "17",

pages = "220--232",

journal = "Plant Biotechnology Journal",

issn = "1467-7644",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "1",

}

Vanhercke, T, Belide, S, Taylor, MC, El Tahchy, A, Okada, S, Rolland, V, Liu, Q, Mitchell, M, Shrestha, P, Venables, I, Ma, L, Blundell, C, Mathew, A, Ziolkowski, L, Niesner, N, Hussain, D, Dong, B, Liu, G, Godwin, ID, Lee, J, Rug, M, Zhou, XR, Singh, SP & Petrie, JR 2019, 'Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor', Plant Biotechnology Journal, vol. 17, no. 1, pp. 220-232. https://doi.org/10.1111/pbi.12959

TY - JOUR

T1 - Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor

AU - Vanhercke, Thomas

AU - Belide, Srinivas

AU - Taylor, Matthew C.

AU - El Tahchy, Anna

AU - Okada, Shoko

AU - Rolland, Vivien

AU - Liu, Qing

AU - Mitchell, Madeline

AU - Shrestha, Pushkar

AU - Venables, Ingrid

AU - Ma, Lina

AU - Blundell, Cheryl

AU - Mathew, Anu

AU - Ziolkowski, Lisa

AU - Niesner, Nathalie

AU - Hussain, Dawar

AU - Dong, Bei

AU - Liu, Guoquan

AU - Godwin, Ian D.

AU - Lee, Jiwon

AU - Rug, Melanie

AU - Zhou, Xue Rong

AU - Singh, Surinder P.

AU - Petrie, James R.

PY - 2019/1

Y1 - 2019/1

N2 - Synthesis and accumulation of the storage lipid triacylglycerol in vegetative plant tissues has emerged as a promising strategy to meet the world's future need for vegetable oil. Sorghum (Sorghum bicolor) is a particularly attractive target crop given its high biomass, drought resistance and C 4 photosynthesis. While oilseed-like triacylglycerol levels have been engineered in the C 3 model plant tobacco, progress in C 4 monocot crops has been lagging behind. In this study, we report the accumulation of triacylglycerol in sorghum leaf tissues to levels between 3 and 8.4% on a dry weight basis depending on leaf and plant developmental stage. This was achieved by the combined overexpression of genes encoding the Zea mays WRI1 transcription factor, Umbelopsis ramanniana UrDGAT2a acyltransferase and Sesamum indicum Oleosin-L oil body protein. Increased oil content was visible as lipid droplets, primarily in the leaf mesophyll cells. A comparison between a constitutive and mesophyll-specific promoter driving WRI1 expression revealed distinct changes in the overall leaf lipidome as well as transitory starch and soluble sugar levels. Metabolome profiling uncovered changes in the abundance of various amino acids and dicarboxylic acids. The results presented here are a first step forward towards the development of sorghum as a dedicated biomass oil crop and provide a basis for further combinatorial metabolic engineering.

AB - Synthesis and accumulation of the storage lipid triacylglycerol in vegetative plant tissues has emerged as a promising strategy to meet the world's future need for vegetable oil. Sorghum (Sorghum bicolor) is a particularly attractive target crop given its high biomass, drought resistance and C 4 photosynthesis. While oilseed-like triacylglycerol levels have been engineered in the C 3 model plant tobacco, progress in C 4 monocot crops has been lagging behind. In this study, we report the accumulation of triacylglycerol in sorghum leaf tissues to levels between 3 and 8.4% on a dry weight basis depending on leaf and plant developmental stage. This was achieved by the combined overexpression of genes encoding the Zea mays WRI1 transcription factor, Umbelopsis ramanniana UrDGAT2a acyltransferase and Sesamum indicum Oleosin-L oil body protein. Increased oil content was visible as lipid droplets, primarily in the leaf mesophyll cells. A comparison between a constitutive and mesophyll-specific promoter driving WRI1 expression revealed distinct changes in the overall leaf lipidome as well as transitory starch and soluble sugar levels. Metabolome profiling uncovered changes in the abundance of various amino acids and dicarboxylic acids. The results presented here are a first step forward towards the development of sorghum as a dedicated biomass oil crop and provide a basis for further combinatorial metabolic engineering.

KW - DGAT

KW - Oleosin

KW - Sorghum bicolor

KW - WRI1

KW - leaf

KW - triacylglycerol

UR - http://www.scopus.com/inward/record.url?scp=85050914123&partnerID=8YFLogxK

U2 - 10.1111/pbi.12959

DO - 10.1111/pbi.12959

M3 - Article

SN - 1467-7644

VL - 17

SP - 220

EP - 232

JO - Plant Biotechnology Journal

JF - Plant Biotechnology Journal

IS - 1

ER -

Up-regulation of lipid biosynthesis increases the oil content in leaves of Sorghum bicolor

Abstract

Access to Document

Other files and links

Fingerprint

Cite this