Lipidomic and transcriptomic profiling of developing nodules reveal the essential roles of active glycolysis and fatty acid and membrane lipid biosynthesis in soybean nodulation.

Gaoyang Zhang; Muhammad Z. Ahmad; Beibei Chen; Sehrish Manan; Yuliang Zhang; Huanan Jin; Xuemin Wang; Jian Zhao

doi:10.1111/TPJ.14805

Lipidomic and transcriptomic profiling of developing nodules reveal the essential roles of active glycolysis and fatty acid and membrane lipid biosynthesis in soybean nodulation.

Gaoyang Zhang, Muhammad Z. Ahmad, Beibei Chen, Sehrish Manan, Yuliang Zhang, Huanan Jin, Xuemin Wang, Jian Zhao

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

Abstract

<div class="line" id="line-15"> Symbiotic rhizobia&hyphen;legume interactions are energy&hyphen;demanding processes, and the carbon supply from host cells that is critically required for nodulation and nitrogen fixation is not fully understood. Investigation of the lipidomic and carbohydrate profiles with the transcriptome of developing nodules revealed highly activated glycolysis, fatty acid (FA), 2&hyphen;monoacylglycerol (2&hyphen;MAG), and membrane lipid biosynthesis and transport during nodule development. RNA&hyphen;sequence profiling of metabolic genes in roots and developing nodules highlighted the enhanced expression of genes involved in the biosynthesis and transport of FAs, membrane lipids, and 2&hyphen;MAG in rhizobia&hyphen;soybean symbioses via the RAML&hyphen;WRI&hyphen;FatM&hyphen;GPAT&hyphen;STRL pathway, which is similar to that in legume&hyphen;arbuscular mycorrhizal fungi symbiosis. The essential roles of the metabolic pathway during soybean nodulation were further supported by analysis of transgenic hairy roots overexpressing soybean  GmWRI1b &hyphen;OE and  GmLEC2a &hyphen;OE.  GmLEC2a &hyphen;OE hairy roots produced fewer nodules, in contrast to  GmWRI1b &hyphen;OE hairy roots.  GmLEC2a &hyphen;OE hairy roots displayed different or even opposite expression patterns of the genes involved in glycolysis and the synthesis of FAs, 2&hyphen;MAG, TAG, and membrane lipids compared to  GmWRI1b &hyphen;OE hairy roots. Glycolysis, FA and membrane lipid biosynthesis were repressed in  GmLEC2a&hyphen;OE  but increased in  GmWRI1b &hyphen;OE hairy roots, which may account for the reduced nodulation in  GmLEC2a&hyphen;OE  hairy roots but increased nodulation in  GmWRI1b &hyphen;OE hairy roots. These data show that active FA, 2&hyphen;MAG and membrane lipid biosynthesis are essential for nodulation and rhizobia&hyphen;soybean symbioses. These data shed light on essential and complex lipid metabolism for soybean nodulation and nodule development, laying the foundation for the future detailed investigation of soybean nodulation. </div>

Original language	American English
Journal	Plant Journal
DOIs	https://doi.org/10.1111/TPJ.14805
State	Published - May 15 2020
Externally published	Yes

Keywords

fatty acid synthesis
lipid metabolism
lipidomics
nodulation
transcription factor
transcriptomic analysis

Disciplines

Biology
Biochemistry

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@article{8a2d7ab7a35c4d4392e9f5184ac7d970,

title = "Lipidomic and transcriptomic profiling of developing nodules reveal the essential roles of active glycolysis and fatty acid and membrane lipid biosynthesis in soybean nodulation.",

abstract = " Symbiotic rhizobia&hyphen;legume interactions are energy&hyphen;demanding processes, and the carbon supply from host cells that is critically required for nodulation and nitrogen fixation is not fully understood. Investigation of the lipidomic and carbohydrate profiles with the transcriptome of developing nodules revealed highly activated glycolysis, fatty acid (FA), 2&hyphen;monoacylglycerol (2&hyphen;MAG), and membrane lipid biosynthesis and transport during nodule development. RNA&hyphen;sequence profiling of metabolic genes in roots and developing nodules highlighted the enhanced expression of genes involved in the biosynthesis and transport of FAs, membrane lipids, and 2&hyphen;MAG in rhizobia&hyphen;soybean symbioses via the RAML&hyphen;WRI&hyphen;FatM&hyphen;GPAT&hyphen;STRL pathway, which is similar to that in legume&hyphen;arbuscular mycorrhizal fungi symbiosis. The essential roles of the metabolic pathway during soybean nodulation were further supported by analysis of transgenic hairy roots overexpressing soybean  GmWRI1b &hyphen;OE and  GmLEC2a &hyphen;OE.  GmLEC2a &hyphen;OE hairy roots produced fewer nodules, in contrast to  GmWRI1b &hyphen;OE hairy roots.  GmLEC2a &hyphen;OE hairy roots displayed different or even opposite expression patterns of the genes involved in glycolysis and the synthesis of FAs, 2&hyphen;MAG, TAG, and membrane lipids compared to  GmWRI1b &hyphen;OE hairy roots. Glycolysis, FA and membrane lipid biosynthesis were repressed in  GmLEC2a&hyphen;OE  but increased in  GmWRI1b &hyphen;OE hairy roots, which may account for the reduced nodulation in  GmLEC2a&hyphen;OE  hairy roots but increased nodulation in  GmWRI1b &hyphen;OE hairy roots. These data show that active FA, 2&hyphen;MAG and membrane lipid biosynthesis are essential for nodulation and rhizobia&hyphen;soybean symbioses. These data shed light on essential and complex lipid metabolism for soybean nodulation and nodule development, laying the foundation for the future detailed investigation of soybean nodulation. ",

keywords = "fatty acid synthesis, lipid metabolism, lipidomics, nodulation, transcription factor, transcriptomic analysis",

author = "Gaoyang Zhang and Ahmad, {Muhammad Z.} and Beibei Chen and Sehrish Manan and Yuliang Zhang and Huanan Jin and Xuemin Wang and Jian Zhao",

note = "Cookies are disabled for this browser. Wiley Online Library requires cookies for authentication and use of other site features; therefore, cookies must be enabled to browse the site. Detailed information on how Wiley uses cookies can be found in our Privacy Policy.",

year = "2020",

month = may,

day = "15",

doi = "10.1111/TPJ.14805",

language = "American English",

journal = "Plant Journal",

}

TY - JOUR

T1 - Lipidomic and transcriptomic profiling of developing nodules reveal the essential roles of active glycolysis and fatty acid and membrane lipid biosynthesis in soybean nodulation.

AU - Zhang, Gaoyang

AU - Ahmad, Muhammad Z.

AU - Chen, Beibei

AU - Manan, Sehrish

AU - Zhang, Yuliang

AU - Jin, Huanan

AU - Wang, Xuemin

AU - Zhao, Jian

N1 - Cookies are disabled for this browser. Wiley Online Library requires cookies for authentication and use of other site features; therefore, cookies must be enabled to browse the site. Detailed information on how Wiley uses cookies can be found in our Privacy Policy.

PY - 2020/5/15

Y1 - 2020/5/15

N2 - Symbiotic rhizobia&hyphen;legume interactions are energy&hyphen;demanding processes, and the carbon supply from host cells that is critically required for nodulation and nitrogen fixation is not fully understood. Investigation of the lipidomic and carbohydrate profiles with the transcriptome of developing nodules revealed highly activated glycolysis, fatty acid (FA), 2&hyphen;monoacylglycerol (2&hyphen;MAG), and membrane lipid biosynthesis and transport during nodule development. RNA&hyphen;sequence profiling of metabolic genes in roots and developing nodules highlighted the enhanced expression of genes involved in the biosynthesis and transport of FAs, membrane lipids, and 2&hyphen;MAG in rhizobia&hyphen;soybean symbioses via the RAML&hyphen;WRI&hyphen;FatM&hyphen;GPAT&hyphen;STRL pathway, which is similar to that in legume&hyphen;arbuscular mycorrhizal fungi symbiosis. The essential roles of the metabolic pathway during soybean nodulation were further supported by analysis of transgenic hairy roots overexpressing soybean  GmWRI1b &hyphen;OE and  GmLEC2a &hyphen;OE.  GmLEC2a &hyphen;OE hairy roots produced fewer nodules, in contrast to  GmWRI1b &hyphen;OE hairy roots.  GmLEC2a &hyphen;OE hairy roots displayed different or even opposite expression patterns of the genes involved in glycolysis and the synthesis of FAs, 2&hyphen;MAG, TAG, and membrane lipids compared to  GmWRI1b &hyphen;OE hairy roots. Glycolysis, FA and membrane lipid biosynthesis were repressed in  GmLEC2a&hyphen;OE  but increased in  GmWRI1b &hyphen;OE hairy roots, which may account for the reduced nodulation in  GmLEC2a&hyphen;OE  hairy roots but increased nodulation in  GmWRI1b &hyphen;OE hairy roots. These data show that active FA, 2&hyphen;MAG and membrane lipid biosynthesis are essential for nodulation and rhizobia&hyphen;soybean symbioses. These data shed light on essential and complex lipid metabolism for soybean nodulation and nodule development, laying the foundation for the future detailed investigation of soybean nodulation.

AB - Symbiotic rhizobia&hyphen;legume interactions are energy&hyphen;demanding processes, and the carbon supply from host cells that is critically required for nodulation and nitrogen fixation is not fully understood. Investigation of the lipidomic and carbohydrate profiles with the transcriptome of developing nodules revealed highly activated glycolysis, fatty acid (FA), 2&hyphen;monoacylglycerol (2&hyphen;MAG), and membrane lipid biosynthesis and transport during nodule development. RNA&hyphen;sequence profiling of metabolic genes in roots and developing nodules highlighted the enhanced expression of genes involved in the biosynthesis and transport of FAs, membrane lipids, and 2&hyphen;MAG in rhizobia&hyphen;soybean symbioses via the RAML&hyphen;WRI&hyphen;FatM&hyphen;GPAT&hyphen;STRL pathway, which is similar to that in legume&hyphen;arbuscular mycorrhizal fungi symbiosis. The essential roles of the metabolic pathway during soybean nodulation were further supported by analysis of transgenic hairy roots overexpressing soybean  GmWRI1b &hyphen;OE and  GmLEC2a &hyphen;OE.  GmLEC2a &hyphen;OE hairy roots produced fewer nodules, in contrast to  GmWRI1b &hyphen;OE hairy roots.  GmLEC2a &hyphen;OE hairy roots displayed different or even opposite expression patterns of the genes involved in glycolysis and the synthesis of FAs, 2&hyphen;MAG, TAG, and membrane lipids compared to  GmWRI1b &hyphen;OE hairy roots. Glycolysis, FA and membrane lipid biosynthesis were repressed in  GmLEC2a&hyphen;OE  but increased in  GmWRI1b &hyphen;OE hairy roots, which may account for the reduced nodulation in  GmLEC2a&hyphen;OE  hairy roots but increased nodulation in  GmWRI1b &hyphen;OE hairy roots. These data show that active FA, 2&hyphen;MAG and membrane lipid biosynthesis are essential for nodulation and rhizobia&hyphen;soybean symbioses. These data shed light on essential and complex lipid metabolism for soybean nodulation and nodule development, laying the foundation for the future detailed investigation of soybean nodulation.

KW - fatty acid synthesis

KW - lipid metabolism

KW - lipidomics

KW - nodulation

KW - transcription factor

KW - transcriptomic analysis

UR - https://www.onlinelibrary.wiley.com/doi/abs/10.1111/tpj.14805

U2 - 10.1111/TPJ.14805

DO - 10.1111/TPJ.14805

M3 - Article

JO - Plant Journal

JF - Plant Journal

ER -

Lipidomic and transcriptomic profiling of developing nodules reveal the essential roles of active glycolysis and fatty acid and membrane lipid biosynthesis in soybean nodulation.

Abstract

Keywords

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