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

Title: Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max)

Abstract

It has been reported that lipid biosynthesis in plant host root cells plays critical roles in legumefungal or -rhizobial symbioses, but little is known about its regulatory mechanism in legume– rhizobia interaction. Soybean WRINKLED1 (WRI1) a and b, with their alternative splicing (AS) products a’ and b’, are highly expressed in developing seeds and nodules, but their functions in soybean nodulation are not known. GmWRI1a and b differently promoted triacylglycerol (TAG) accumulation in both Arabidopsis wild-type and wri1 mutant seeds and when they ectopically expressed in the soybean hairy roots. Transcriptome analysis revealed that 15 genes containing AW boxes in their promoters were targeted by GmWRI1s, including genes involved in glycolysis, fatty acid (FA) and TAG biosynthesis. GmWRI1a, GmWRI1b and b’ differentially transactivated most targeted genes. Overexpression of GmWRI1s affected phospholipid and galactolipid synthesis, soluble sugar and starch contents and led to increased nodule numbers, whereas GmWRI1 knockdown hairy roots interfered root glycolysis and lipid biosynthesis and resulted in fewer nodules. These phenomena in GmWRI1 mutants coincided with the altered expression of nodulation genes. Thus, GmWRI1-regulated starch degradation, glycolysis and lipid biosynthesis were critical for nodulation. GmWRI1 mutants also altered auxin and other hormone-related biosynthesis and hormone-related genes, by whichmore » GmWRI1s may affect nodule development. The study expands the views for pleiotropic effects of WRI1s in regulating soybean seed filling and root nodulation.« less

Authors:
 [1];  [2];  [2];  [2]; ORCiD logo [1];  [3];  [4]; ORCiD logo [2]
  1. Huazhong Agricultural Univ., Wuhan (China)
  2. Anhui Agricultural Univ., Hefei (China)
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  4. Univ. of Missouri, St. Louis, MO (United States); Donald Danforth Plant Science Center, St. Louis, MO (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1607872
Alternate Identifier(s):
OSTI ID: 1735816
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 18; Journal Issue: 1; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbon partitioning; lipid biosynthesis; transcriptional regulation; glycolysis; alternative splicing; nodulation; carbon partitioning, lipid biosynthesis, transcriptional regulation, glycolysis, alternative splicing, nodulation.

Citation Formats

Chen, Beibei, Zhang, Gaoyang, Li, Penghui, Yang, Jihong, Guo, Liang, Benning, Christoph, Wang, Xuemin, and Zhao, Jian. Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max). United States: N. p., 2019. Web. doi:10.1111/pbi.13183.
Chen, Beibei, Zhang, Gaoyang, Li, Penghui, Yang, Jihong, Guo, Liang, Benning, Christoph, Wang, Xuemin, & Zhao, Jian. Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max). United States. https://doi.org/10.1111/pbi.13183
Chen, Beibei, Zhang, Gaoyang, Li, Penghui, Yang, Jihong, Guo, Liang, Benning, Christoph, Wang, Xuemin, and Zhao, Jian. Mon . "Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max)". United States. https://doi.org/10.1111/pbi.13183. https://www.osti.gov/servlets/purl/1607872.
@article{osti_1607872,
title = {Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max)},
author = {Chen, Beibei and Zhang, Gaoyang and Li, Penghui and Yang, Jihong and Guo, Liang and Benning, Christoph and Wang, Xuemin and Zhao, Jian},
abstractNote = {It has been reported that lipid biosynthesis in plant host root cells plays critical roles in legumefungal or -rhizobial symbioses, but little is known about its regulatory mechanism in legume– rhizobia interaction. Soybean WRINKLED1 (WRI1) a and b, with their alternative splicing (AS) products a’ and b’, are highly expressed in developing seeds and nodules, but their functions in soybean nodulation are not known. GmWRI1a and b differently promoted triacylglycerol (TAG) accumulation in both Arabidopsis wild-type and wri1 mutant seeds and when they ectopically expressed in the soybean hairy roots. Transcriptome analysis revealed that 15 genes containing AW boxes in their promoters were targeted by GmWRI1s, including genes involved in glycolysis, fatty acid (FA) and TAG biosynthesis. GmWRI1a, GmWRI1b and b’ differentially transactivated most targeted genes. Overexpression of GmWRI1s affected phospholipid and galactolipid synthesis, soluble sugar and starch contents and led to increased nodule numbers, whereas GmWRI1 knockdown hairy roots interfered root glycolysis and lipid biosynthesis and resulted in fewer nodules. These phenomena in GmWRI1 mutants coincided with the altered expression of nodulation genes. Thus, GmWRI1-regulated starch degradation, glycolysis and lipid biosynthesis were critical for nodulation. GmWRI1 mutants also altered auxin and other hormone-related biosynthesis and hormone-related genes, by which GmWRI1s may affect nodule development. The study expands the views for pleiotropic effects of WRI1s in regulating soybean seed filling and root nodulation.},
doi = {10.1111/pbi.13183},
journal = {Plant Biotechnology Journal},
number = 1,
volume = 18,
place = {United States},
year = {Mon Jun 03 00:00:00 EDT 2019},
month = {Mon Jun 03 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 45 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol
journal, June 2010

  • Yang, W.; Pollard, M.; Li-Beisson, Y.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 26
  • DOI: 10.1073/pnas.0914149107

A Soybean Acyl Carrier Protein, GmACP, Is Important for Root Nodule Symbiosis
journal, May 2014

  • Wang, Jun; Tóth, Katalin; Tanaka, Kiwamu
  • Molecular Plant-Microbe Interactions, Vol. 27, Issue 5
  • DOI: 10.1094/MPMI-09-13-0269-R

A Common Signaling Process that Promotes Mycorrhizal and Oomycete Colonization of Plants
journal, December 2012


A GRAS-Type Transcription Factor with a Specific Function in Mycorrhizal Signaling
journal, December 2012


Diverse functions of multidrug and toxin extrusion (MATE) transporters in citric acid efflux and metal homeostasis in Medicago truncatula
journal, February 2017

  • Wang, Junjie; Hou, Qiuqiang; Li, Penghui
  • The Plant Journal, Vol. 90, Issue 1
  • DOI: 10.1111/tpj.13471

Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis
journal, February 2011


BnWRI1 coordinates fatty acid biosynthesis and photosynthesis pathways during oil accumulation in rapeseed
journal, March 2014

  • Wu, Xue-Long; Liu, Zhi-Hong; Hu, Zhang-Hua
  • Journal of Integrative Plant Biology, Vol. 56, Issue 6
  • DOI: 10.1111/jipb.12158

Complexity of the Alternative Splicing Landscape in Plants
journal, October 2013

  • Reddy, Anireddy S. N.; Marquez, Yamile; Kalyna, Maria
  • The Plant Cell, Vol. 25, Issue 10
  • DOI: 10.1105/tpc.113.117523

Lipid transfer from plants to arbuscular mycorrhiza fungi
journal, July 2017


Structural insights into alternative splicing-mediated desensitization of jasmonate signaling
journal, January 2017

  • Zhang, Feng; Ke, Jiyuan; Zhang, Li
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 7
  • DOI: 10.1073/pnas.1616938114

Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi
journal, June 2017


Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant
journal, June 2017

  • Luginbuehl, Leonie H.; Menard, Guillaume N.; Kurup, Smita
  • Science, Vol. 356, Issue 6343
  • DOI: 10.1126/science.aan0081

MtLAX2, a Functional Homologue of the Arabidopsis Auxin Influx Transporter AUX1, Is Required for Nodule Organogenesis
journal, March 2017

  • Roy, Sonali; Robson, Fran; Lilley, Jodi
  • Plant Physiology, Vol. 174, Issue 1
  • DOI: 10.1104/pp.16.01473

Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume
journal, October 2006

  • Heckmann, Anne B.; Lombardo, Fabien; Miwa, Hiroki
  • Plant Physiology, Vol. 142, Issue 4
  • DOI: 10.1104/pp.106.089508

V ARIATIONS IN THE B IOSYNTHESIS OF S EED -S TORAGE L IPIDS
journal, June 2001


The Medicago truncatula N5 Gene Encoding a Root-Specific Lipid Transfer Protein Is Required for the Symbiotic Interaction with Sinorhizobium meliloti
journal, December 2009

  • Pii, Youry; Astegno, Alessandra; Peroni, Elisa
  • Molecular Plant-Microbe Interactions, Vol. 22, Issue 12
  • DOI: 10.1094/MPMI-22-12-1577

Expression of ZmLEC1 and ZmWRI1 Increases Seed Oil Production in Maize
journal, May 2010

  • Shen, Bo; Allen, William B.; Zheng, Peizhong
  • Plant Physiology, Vol. 153, Issue 3
  • DOI: 10.1104/pp.110.157537

WRINKLED1, A Ubiquitous Regulator in Oil Accumulating Tissues from Arabidopsis Embryos to Oil Palm Mesocarp
journal, July 2013


Transport and transcriptional regulation of oil production in plants
journal, August 2016


Metabolic engineering of proanthocyanidin production by repressing the isoflavone pathways and redirecting anthocyanidin precursor flux in legume
journal, January 2016

  • Li, Penghui; Dong, Qiang; Ge, Shujun
  • Plant Biotechnology Journal, Vol. 14, Issue 7
  • DOI: 10.1111/pbi.12524

Transport and Metabolism in Legume-Rhizobia Symbioses
journal, April 2013


Symbiotic Fungi Control Plant Root Cortex Development through the Novel GRAS Transcription Factor MIG1
journal, October 2016


Functional characterization of soybean strigolactone biosynthesis and signaling genes in Arabidopsis MAX mutants and GmMAX3 in soybean nodulation
journal, December 2017

  • Haq, Basir UI; Ahmad, Muhammad Zulfiqar; ur Rehman, Naveed
  • BMC Plant Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12870-017-1182-4

14-3-3 protein mediates plant seed oil biosynthesis through interaction with AtWRI1
journal, August 2016

  • Ma, Wei; Kong, Que; Mantyla, Jenny J.
  • The Plant Journal, Vol. 88, Issue 2
  • DOI: 10.1111/tpj.13244

Soybean LEC2 Regulates Subsets of Genes Involved in Controlling the Biosynthesis and Catabolism of Seed Storage Substances and Seed Development
journal, September 2017

  • Manan, Sehrish; Ahmad, Muhammad Z.; Zhang, Gaoyang
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01604

AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus
journal, September 2018

  • Xue, Li; Klinnawee, Lompong; Zhou, Yue
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 39
  • DOI: 10.1073/pnas.1812275115

Soybean Metabolites Regulated in Root Hairs in Response to the Symbiotic Bacterium Bradyrhizobium japonicum
journal, June 2010

  • Brechenmacher, Laurent; Lei, Zhentian; Libault, Marc
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.157800

Transport processes of the legume symbiosome membrane
journal, December 2014

  • Clarke, Victoria C.; Loughlin, Patrick C.; Day, David A.
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00699

Biochemical pathways in seed oil synthesis
journal, June 2013

  • Bates, Philip D.; Stymne, Sten; Ohlrogge, John
  • Current Opinion in Plant Biology, Vol. 16, Issue 3
  • DOI: 10.1016/j.pbi.2013.02.015

Membrane Lipids in Plant-Associated Bacteria: Their Biosyntheses and Possible Functions
journal, July 2003

  • López-Lara, Isabel M.; Sohlenkamp, Christian; Geiger, Otto
  • Molecular Plant-Microbe Interactions, Vol. 16, Issue 7
  • DOI: 10.1094/MPMI.2003.16.7.567

Duplicate Maize Wrinkled1 Transcription Factors Activate Target Genes Involved in Seed Oil Biosynthesis
journal, April 2011

  • Pouvreau, Benjamin; Baud, Sébastien; Vernoud, Vanessa
  • Plant Physiology, Vol. 156, Issue 2
  • DOI: 10.1104/pp.111.173641

Alternative Splicing at the Intersection of Biological Timing, Development, and Stress Responses
journal, October 2013


The Galactolipid Digalactosyldiacylglycerol Accumulates in the Peribacteroid Membrane of Nitrogen-fixing Nodules of Soybean and Lotus
journal, May 2004

  • Gaude, Nicole; Tippmann, Helge; Flemetakis, Emmanouil
  • Journal of Biological Chemistry, Vol. 279, Issue 33
  • DOI: 10.1074/jbc.M404098200

Stearoyl-Acyl Carrier Protein Desaturase Mutations Uncover an Impact of Stearic Acid in Leaf and Nodule Structure
journal, May 2017

  • Lakhssassi, Naoufal; Colantonio, Vincent; Flowers, Nicholas D.
  • Plant Physiology, Vol. 174, Issue 3
  • DOI: 10.1104/pp.16.01929

Plasticity and innovation of regulatory mechanisms underlying seed oil content mediated by duplicated genes in the palaeopolyploid soybean
journal, April 2017

  • Zhang, Dajian; Zhao, Meixia; Li, Shuai
  • The Plant Journal, Vol. 90, Issue 6
  • DOI: 10.1111/tpj.13533

Medicago AP2-Domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal Symbiosis
journal, November 2018


Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes
journal, June 2008


Nodule carbohydrate catabolism is enhanced in the Medicago truncatula A17-Sinorhizobium medicae WSM419 symbiosis
journal, August 2014

  • Larrainzar, Estíbaliz; Gil-Quintana, Erena; Seminario, Amaia
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00447

The Arabidopsis WRINKLED1 transcription factor affects auxin homeostasis in roots
journal, July 2017

  • Kong, Que; Ma, Wei; Yang, Haibing
  • Journal of Experimental Botany, Vol. 68, Issue 16
  • DOI: 10.1093/jxb/erx275

Transport and transcriptional regulation of oil production in plants
text, January 2016


Transport and transcriptional regulation of oil production in plants
text, January 2016


A Common Signaling Process that Promotes Mycorrhizal and Oomycete Colonization of Plants
journal, December 2012


A GRAS-Type Transcription Factor with a Specific Function in Mycorrhizal Signaling
journal, December 2012


Symbiotic Fungi Control Plant Root Cortex Development through the Novel GRAS Transcription Factor MIG1
journal, October 2016


Transcriptional Regulation of Nutrient Exchange in Arbuscular Mycorrhizal Symbiosis
journal, December 2018


Biochemical pathways in seed oil synthesis
journal, June 2013

  • Bates, Philip D.; Stymne, Sten; Ohlrogge, John
  • Current Opinion in Plant Biology, Vol. 16, Issue 3
  • DOI: 10.1016/j.pbi.2013.02.015

A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol
journal, June 2010

  • Yang, W.; Pollard, M.; Li-Beisson, Y.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 26
  • DOI: 10.1073/pnas.0914149107

Structural insights into alternative splicing-mediated desensitization of jasmonate signaling
journal, January 2017

  • Zhang, Feng; Ke, Jiyuan; Zhang, Li
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 7
  • DOI: 10.1073/pnas.1616938114

AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus
journal, September 2018

  • Xue, Li; Klinnawee, Lompong; Zhou, Yue
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 39
  • DOI: 10.1073/pnas.1812275115

Transport and transcriptional regulation of oil production in plants
journal, August 2016


The Bacteroid Periplasm in Soybean Nodules Is an Interkingdom Symbiotic Space
journal, December 2017

  • Strodtman, Kent N.; Stevenson, Severin E.; Waters, James K.
  • Molecular Plant-Microbe Interactions, Vol. 30, Issue 12
  • DOI: 10.1094/mpmi-12-16-0264-r

Expression of ZmLEC1 and ZmWRI1 Increases Seed Oil Production in Maize
journal, May 2010

  • Shen, Bo; Allen, William B.; Zheng, Peizhong
  • Plant Physiology, Vol. 153, Issue 3
  • DOI: 10.1104/pp.110.157537

Duplicate Maize Wrinkled1 Transcription Factors Activate Target Genes Involved in Seed Oil Biosynthesis
journal, April 2011

  • Pouvreau, Benjamin; Baud, Sébastien; Vernoud, Vanessa
  • Plant Physiology, Vol. 156, Issue 2
  • DOI: 10.1104/pp.111.173641

Stearoyl-Acyl Carrier Protein Desaturase Mutations Uncover an Impact of Stearic Acid in Leaf and Nodule Structure
journal, May 2017

  • Lakhssassi, Naoufal; Colantonio, Vincent; Flowers, Nicholas D.
  • Plant Physiology, Vol. 174, Issue 3
  • DOI: 10.1104/pp.16.01929

Complexity of the Alternative Splicing Landscape in Plants
journal, October 2013

  • Reddy, Anireddy S. N.; Marquez, Yamile; Kalyna, Maria
  • The Plant Cell, Vol. 25, Issue 10
  • DOI: 10.1105/tpc.113.117523

The Plant Cell Reviews Alternative Splicing
journal, October 2013


Metabolic engineering of proanthocyanidin production by repressing the isoflavone pathways and redirecting anthocyanidin precursor flux in legume
journal, January 2016

  • Li, Penghui; Dong, Qiang; Ge, Shujun
  • Plant Biotechnology Journal, Vol. 14, Issue 7
  • DOI: 10.1111/pbi.12524

Diverse functions of multidrug and toxin extrusion (MATE) transporters in citric acid efflux and metal homeostasis in Medicago truncatula
journal, February 2017

  • Wang, Junjie; Hou, Qiuqiang; Li, Penghui
  • The Plant Journal, Vol. 90, Issue 1
  • DOI: 10.1111/tpj.13471

Plasticity and innovation of regulatory mechanisms underlying seed oil content mediated by duplicated genes in the palaeopolyploid soybean
journal, April 2017

  • Zhang, Dajian; Zhao, Meixia; Li, Shuai
  • The Plant Journal, Vol. 90, Issue 6
  • DOI: 10.1111/tpj.13533

Location, location, location: lipid metabolism varies in different parts of the seed
journal, June 2018


Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi
journal, June 2017


Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant
journal, June 2017

  • Luginbuehl, Leonie H.; Menard, Guillaume N.; Kurup, Smita
  • Science, Vol. 356, Issue 6343
  • DOI: 10.1126/science.aan0081

V ARIATIONS IN THE B IOSYNTHESIS OF S EED -S TORAGE L IPIDS
journal, June 2001


Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes
journal, June 2008


Functional characterization of soybean strigolactone biosynthesis and signaling genes in Arabidopsis MAX mutants and GmMAX3 in soybean nodulation
journal, December 2017

  • Haq, Basir UI; Ahmad, Muhammad Zulfiqar; ur Rehman, Naveed
  • BMC Plant Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12870-017-1182-4

WRINKLED1, A Ubiquitous Regulator in Oil Accumulating Tissues from Arabidopsis Embryos to Oil Palm Mesocarp
journal, July 2013


Soybean LEC2 Regulates Subsets of Genes Involved in Controlling the Biosynthesis and Catabolism of Seed Storage Substances and Seed Development
journal, September 2017

  • Manan, Sehrish; Ahmad, Muhammad Z.; Zhang, Gaoyang
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01604

Works referencing / citing this record:

Molecular Basis of Plant Oil Biosynthesis: Insights Gained From Studying the WRINKLED1 Transcription Factor
journal, February 2020