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Title: Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis

Abstract

Assimilate partitioning to the root system is a desirable developmental trait to control but little is known of the signaling pathway underlying partitioning. A null mutation in the gene encoding the Gβ subunit of the heterotrimeric G protein complex, a nexus for a variety of signaling pathways, confers altered sugar partitioning in roots. While fixed carbon rapidly reached the roots of wild type and agb1-2 mutant seedlings, agb1 roots had more of this fixed carbon in the form of glucose, fructose, and sucrose which manifested as a higher lateral root density. Upon glucose treatment, the agb1-2 mutant had abnormal gene expression in the root tip validated by transcriptome analysis. In addition, PIN2 membrane localization was altered in the agb1-2 mutant. The heterotrimeric G protein complex integrates photosynthesis-derived sugar signaling incorporating both membrane-and transcriptional-based mechanisms. The time constants for these signaling mechanisms are in the same range as photosynthate delivery to the root, raising the possibility that root cells are able to use changes in carbon fixation in real time to adjust growth behavior.

Authors:
 [1];  [2];  [3];  [3];  [3];  [3]
  1. University of Delhi, New Delhi (India); University of North Carolina, Chapel Hill, NC (United States)
  2. Brookhaven National Laboratory (BNL), Upton, NY (United States)
  3. University of North Carolina, Chapel Hill, NC (United States)
Publication Date:
Research Org.:
University of North Carolina, Chapel Hill, NC (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); National Institute of General Medical Sciences (NIGMS); National Science Foundation (NSF); Government of India; Delhi University; Pew Latin American Fellows Program
OSTI Identifier:
1904659
Grant/Contract Number:  
FG02-05ER15671; R01GM065989; MCB-0723515; MCB-1158054; MCB-0718202
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; photosynthetic partitioning; positron electron tomography imaging; AGB1; lateral root density; glucose; gene expression; PIN2-GFP

Citation Formats

Mudgil, Yashwanti, Karve, Abhijit, Teixeira, Paulo J. P. L., Jiang, Kun, Tunc-Ozdemir, Meral, and Jones, Alan M. Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.01255.
Mudgil, Yashwanti, Karve, Abhijit, Teixeira, Paulo J. P. L., Jiang, Kun, Tunc-Ozdemir, Meral, & Jones, Alan M. Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis. United States. https://doi.org/10.3389/fpls.2016.01255
Mudgil, Yashwanti, Karve, Abhijit, Teixeira, Paulo J. P. L., Jiang, Kun, Tunc-Ozdemir, Meral, and Jones, Alan M. Thu . "Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis". United States. https://doi.org/10.3389/fpls.2016.01255. https://www.osti.gov/servlets/purl/1904659.
@article{osti_1904659,
title = {Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis},
author = {Mudgil, Yashwanti and Karve, Abhijit and Teixeira, Paulo J. P. L. and Jiang, Kun and Tunc-Ozdemir, Meral and Jones, Alan M.},
abstractNote = {Assimilate partitioning to the root system is a desirable developmental trait to control but little is known of the signaling pathway underlying partitioning. A null mutation in the gene encoding the Gβ subunit of the heterotrimeric G protein complex, a nexus for a variety of signaling pathways, confers altered sugar partitioning in roots. While fixed carbon rapidly reached the roots of wild type and agb1-2 mutant seedlings, agb1 roots had more of this fixed carbon in the form of glucose, fructose, and sucrose which manifested as a higher lateral root density. Upon glucose treatment, the agb1-2 mutant had abnormal gene expression in the root tip validated by transcriptome analysis. In addition, PIN2 membrane localization was altered in the agb1-2 mutant. The heterotrimeric G protein complex integrates photosynthesis-derived sugar signaling incorporating both membrane-and transcriptional-based mechanisms. The time constants for these signaling mechanisms are in the same range as photosynthate delivery to the root, raising the possibility that root cells are able to use changes in carbon fixation in real time to adjust growth behavior.},
doi = {10.3389/fpls.2016.01255},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Thu Aug 25 00:00:00 EDT 2016},
month = {Thu Aug 25 00:00:00 EDT 2016}
}

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Auxin acts as a local morphogenetic trigger to specify lateral root founder cells
journal, June 2008

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Cytokinin regulates root meristem activity via modulation of the polar auxin transport
journal, February 2009

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  • DOI: 10.1073/pnas.0900060106

Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis
journal, June 2012

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Sugar demand, not auxin, is the initial regulator of apical dominance
journal, April 2014

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  • Annals of Botany, Vol. 97, Issue 5
  • DOI: 10.1093/aob/mcj604

Form matters: morphological aspects of lateral root development
journal, November 2013


TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


A model system to study the effects of elevated CO2 on the developmental physiology of roots: the use of Arabidopsis thaliana
journal, March 1998

  • Crookshanks, M.; Taylor, G.; Dolan, L.
  • Journal of Experimental Botany, Vol. 49, Issue 320
  • DOI: 10.1093/jxb/49.320.593

PlantGSEA: a gene set enrichment analysis toolkit for plant community
journal, April 2013

  • Yi, Xin; Du, Zhou; Su, Zhen
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt281

Radio-Metabolite Analysis of Carbon-11 Biochemical Partitioning to Non-Structural Carbohydrates for Integrated Metabolism and Transport Studies
journal, April 2013

  • Babst, Benjamin A.; Karve, Abhijit A.; Judt, Tatjana
  • Plant and Cell Physiology, Vol. 54, Issue 6
  • DOI: 10.1093/pcp/pct045

High CO2 Triggers Preferential Root Growth of Arabidopsis thaliana Via Two Distinct Systems Under Low pH and Low N Stresses
journal, January 2014

  • Hachiya, Takushi; Sugiura, Daisuke; Kojima, Mikiko
  • Plant and Cell Physiology, Vol. 55, Issue 2
  • DOI: 10.1093/pcp/pcu001

Heterotrimeric G protein signalling in the plant kingdom
journal, March 2013

  • Urano, Daisuke; Chen, Jin-Gui; Botella, José Ramón
  • Open Biology, Vol. 3, Issue 3
  • DOI: 10.1098/rsob.120186

Dissecting the effects of nitrate, sucrose and osmotic potential on Arabidopsis root and shoot system growth in laboratory assays
journal, June 2012

  • Roycewicz, Peter; Malamy, Jocelyn E.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1595
  • DOI: 10.1098/rstb.2011.0230

Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots
journal, May 2006

  • Chen, Jin-Gui; Gao, Yajun; Jones, Alan M.
  • Plant Physiology, Vol. 141, Issue 3
  • DOI: 10.1104/pp.106.079202

An Endogenous Carbon-Sensing Pathway Triggers Increased Auxin Flux and Hypocotyl Elongation      
journal, October 2012

  • Lilley, Jodi L. Stewart; Gee, Christopher W.; Sairanen, Ilkka
  • Plant Physiology, Vol. 160, Issue 4
  • DOI: 10.1104/pp.112.205575

Temporal Changes in Allocation and Partitioning of New Carbon as 11 C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis
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Works referencing / citing this record:

Long-distance communication in Arabidopsis involving a self-activating G protein
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Deficit Alternate Drip Irrigation Increased Root-Soil-Plant Interaction, Tomato Yield, and Quality
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Sweet Immunity: Inulin Boosts Resistance of Lettuce (Lactuca sativa) against Grey Mold (Botrytis cinerea) in an Ethylene-Dependent Manner
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