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Title: Multi-omics approach identifies molecular mechanisms of plant-fungus mycorrhizal interaction

Abstract

In mycorrhizal symbiosis, plant roots form close, mutually beneficial interactions with soil fungi. Before this mycorrhizal interaction can be established however, plant roots must be capable of detecting potential beneficial fungal partners and initiating the gene expression patterns necessary to begin symbiosis. To predict a plant root – mycorrhizal fungi sensor systems, we analyzed in vitro experiments of Populus tremuloides (aspen tree) and Laccaria bicolor (mycorrhizal fungi) interaction and leveraged over 200 previously published transcriptomic experimental data sets, 159 experimentally validated plant transcription factor binding motifs, and more than 120-thousand experimentally validated protein-protein interactions to generate models of pre-mycorrhizal sensor systems in aspen root. These sensor mechanisms link extracellular signaling molecules with gene regulation through a network comprised of membrane receptors, signal cascade proteins, transcription factors, and transcription factor biding DNA motifs. Modeling predicted four pre-mycorrhizal sensor complexes in aspen that interact with fifteen transcription factors to regulate the expression of 1184 genes in response to extracellular signals synthesized by Laccaria. Predicted extracellular signaling molecules include common signaling molecules such as phenylpropanoids, salicylate, and, jasmonic acid. Lastly, this multi-omic computational modeling approach for predicting the complex sensory networks yielded specific, testable biological hypotheses for mycorrhizal interaction signaling compounds, sensor complexes,more » and mechanisms of gene regulation.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [2];  [3]
  1. Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Illinois, Chicago, IL (United States)
  2. Univ. of Alabama in Huntsville, Huntsville, AL (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States)
  4. Univ. of Illinois, Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1248919
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Laccaria bicolor; Populus tremuloides; metabolomics; mycorrhizae; proteomics; system modeling; transcriptomics

Citation Formats

Larsen, Peter E., Sreedasyam, Avinash, Trivedi, Geetika, Desai, Shalaka D., Dai, Yang, Cseke, Leland, and Collart, Frank R. Multi-omics approach identifies molecular mechanisms of plant-fungus mycorrhizal interaction. United States: N. p., 2016. Web. doi:10.3389/fpls.2015.01061.
Larsen, Peter E., Sreedasyam, Avinash, Trivedi, Geetika, Desai, Shalaka D., Dai, Yang, Cseke, Leland, & Collart, Frank R. Multi-omics approach identifies molecular mechanisms of plant-fungus mycorrhizal interaction. United States. https://doi.org/10.3389/fpls.2015.01061
Larsen, Peter E., Sreedasyam, Avinash, Trivedi, Geetika, Desai, Shalaka D., Dai, Yang, Cseke, Leland, and Collart, Frank R. Tue . "Multi-omics approach identifies molecular mechanisms of plant-fungus mycorrhizal interaction". United States. https://doi.org/10.3389/fpls.2015.01061. https://www.osti.gov/servlets/purl/1248919.
@article{osti_1248919,
title = {Multi-omics approach identifies molecular mechanisms of plant-fungus mycorrhizal interaction},
author = {Larsen, Peter E. and Sreedasyam, Avinash and Trivedi, Geetika and Desai, Shalaka D. and Dai, Yang and Cseke, Leland and Collart, Frank R.},
abstractNote = {In mycorrhizal symbiosis, plant roots form close, mutually beneficial interactions with soil fungi. Before this mycorrhizal interaction can be established however, plant roots must be capable of detecting potential beneficial fungal partners and initiating the gene expression patterns necessary to begin symbiosis. To predict a plant root – mycorrhizal fungi sensor systems, we analyzed in vitro experiments of Populus tremuloides (aspen tree) and Laccaria bicolor (mycorrhizal fungi) interaction and leveraged over 200 previously published transcriptomic experimental data sets, 159 experimentally validated plant transcription factor binding motifs, and more than 120-thousand experimentally validated protein-protein interactions to generate models of pre-mycorrhizal sensor systems in aspen root. These sensor mechanisms link extracellular signaling molecules with gene regulation through a network comprised of membrane receptors, signal cascade proteins, transcription factors, and transcription factor biding DNA motifs. Modeling predicted four pre-mycorrhizal sensor complexes in aspen that interact with fifteen transcription factors to regulate the expression of 1184 genes in response to extracellular signals synthesized by Laccaria. Predicted extracellular signaling molecules include common signaling molecules such as phenylpropanoids, salicylate, and, jasmonic acid. Lastly, this multi-omic computational modeling approach for predicting the complex sensory networks yielded specific, testable biological hypotheses for mycorrhizal interaction signaling compounds, sensor complexes, and mechanisms of gene regulation.},
doi = {10.3389/fpls.2015.01061},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Tue Jan 19 00:00:00 EST 2016},
month = {Tue Jan 19 00:00:00 EST 2016}
}

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journal, February 2008


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journal, July 2002

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Comprehensive Comparison of Auxin-Regulated and Brassinosteroid-Regulated Genes in Arabidopsis
journal, March 2004

  • Goda, Hideki; Sawa, Shinichiro; Asami, Tadao
  • Plant Physiology, Vol. 134, Issue 4
  • DOI: 10.1104/pp.103.034736

Genome-Wide Identification of Potential Plant E2F Target Genes
journal, August 2005

  • Vandepoele, Klaas; Vlieghe, Kobe; Florquin, Kobe
  • Plant Physiology, Vol. 139, Issue 1
  • DOI: 10.1104/pp.105.066290

Tissue-Specific and Development-Dependent Accumulation of Phenylpropanoids in Larch Mycorrhizas
journal, May 1997

  • Weiss, M.; Mikolajewski, S.; Peipp, H.
  • Plant Physiology, Vol. 114, Issue 1
  • DOI: 10.1104/pp.114.1.15

Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) Function as Transcriptional Activators in Abscisic Acid Signaling
journal, December 2002

  • Abe, Hiroshi; Urao, Takeshi; Ito, Takuya
  • The Plant Cell, Vol. 15, Issue 1
  • DOI: 10.1105/tpc.006130

Regulatory Elements of the Floral Homeotic Gene AGAMOUS Identified by Phylogenetic Footprinting and Shadowing
journal, May 2003

  • Hong, Ray L.; Hamaguchi, Lynn; Busch, Maximilian A.
  • The Plant Cell, Vol. 15, Issue 6
  • DOI: 10.1105/tpc.009548

CONSTANS and the CCAAT Box Binding Complex Share a Functionally Important Domain and Interact to Regulate Flowering of Arabidopsis
journal, November 2006

  • Wenkel, Stephan; Turck, Franziska; Singer, Kamy
  • The Plant Cell, Vol. 18, Issue 11
  • DOI: 10.1105/tpc.106.043299

Bacterial Cyclic β-(1,2)-Glucan Acts in Systemic Suppression of Plant Immune Responses
journal, June 2007

  • Rigano, Luciano Ariel; Payette, Caroline; Brouillard, Geneviève
  • The Plant Cell, Vol. 19, Issue 6
  • DOI: 10.1105/tpc.106.047944

Arabidopsis Ethylene-Responsive Element Binding Factors Act as Transcriptional Activators or Repressors of GCC Box–Mediated Gene Expression
journal, March 2000

  • Fujimoto, Susan Y.; Ohta, Masaru; Usui, Akemi
  • The Plant Cell, Vol. 12, Issue 3
  • DOI: 10.1105/tpc.12.3.393

Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato
journal, December 2007


Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure
journal, April 2005


The Laccaria genome: a symbiont blueprint decoded
journal, October 2008


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate
journal, July 2010


Molecular genetics of plant disease resistance
journal, May 1995


Plant Immunity to Insect Herbivores
journal, June 2008


Light-Regulated Transcription
journal, June 1995


A statistical method to incorporate biological knowledge for generating testable novel gene regulatory interactions from microarray experiments
journal, January 2007


Rank-based edge reconstruction for scale-free genetic regulatory networks
journal, January 2008


Glycosylation-mediated phenylpropanoid partitioning in Populus tremuloides cell cultures
journal, January 2009

  • Payyavula, Raja S.; Babst, Benjamin A.; Nelsen, Matthew P.
  • BMC Plant Biology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2229-9-151

Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome
journal, January 2011

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Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation
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